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Functional neuroimaging using MRI relies on measurements of blood oxygen level-dependent (BOLD) signals from which inferences are made about the underlying neuronal activity. This is possible because neuronal activity elicits increases in blood flow via neurovascular coupling, which gives rise to the BOLD signal. Hence, an accurate interpretation of what BOLD signals mean in terms of neural activity depends on a full understanding of the mechanisms that underlie the measured signal, including neurovascular and neurometabolic coupling, the contribution of different cell types to local signalling, and regional differences in these mechanisms. Furthermore, the contributions of systemic functions to cerebral blood flow may vary with ageing, disease and arousal states, with regard to both neuronal and vascular function. In addition, recent developments in non-invasive imaging technology, such as high-field fMRI, and comparative inter-species analysis, allow connections between non-invasive data and mechanistic knowledge gained from invasive cellular-level studies. Considered together, these factors have immense potential to improve BOLD signal interpretation and bring us closer to the ultimate purpose of decoding the mechanisms of human cognition. This theme issue covers a range of recent advances in these topics, providing a multidisciplinary scientific and technical framework for future work in the neurovascular and cognitive sciences. This article is part of the theme issue ‘Key relationships between non-invasive functional neuroimaging and the underlying neuronal activity'.

During a Research Career Development Award from the National Eye Institute, I spent a year at the University of Cambridge doing research with John Robson. The goal was to use a visual stimulation approach that had not been previously attempted, with the intention of exploring fundamental organization principles of the neural basis of binocular vision. The idea was to use sinusoidal gratings that drifted before both eyes such that the relative phase for one eye was fixed while that of the other was varied. This provided binocular stimuli of variable relative phase, i.e. retinal disparity, to enable testing of binocular response characteristics. We were able to obtain different types of disparity tuning functions for neurons in the primary visual cortex. This work, followed by extended investigations in Berkeley, provided basic information regarding response characteristics of simple and complex cells. We have also shown for monocular deprivation, an approximate model for human amblyopia, that many neurons remain connected to the deprived eye, as demonstrated with dichoptic activation. A selected portion of this work is described here.

Non-invasive brain imaging requires comprehensive interpretation of hemodynamic signals. In functional magnetic resonance imaging, blood oxygen level dependent (BOLD) signals are used to infer neural processes. This necessitates a clear understanding of how BOLD signals and neural activity are related. One fundamental question concerns the relative importance of synaptic activity and spiking discharge. Although these two components are related, most previous work shows that synaptic activity is better reflected in the BOLD signal. However, the mechanisms of this relationship are not clear. The BOLD signal depends on relative changes in cerebral blood flow and cerebral metabolic rate of oxygen. Oxygen metabolism changes are difficult to measure with current imaging techniques, but it is possible to obtain direct quantitative simultaneous in vivo measurement of tissue oxygen and co-localized underlying neural activity. Here, we use this approach with a specific binocular stimulus protocol in order to activate inhibitory and excitatory neuronal pathways in visual cortex. During excitatory binocular interaction, we find that metabolic, spiking, and local field potential responses are correlated. However, during suppressive binocular interaction, spiking activity and local field potentials are dissociated while only the latter is coupled with metabolic response. These results suggest that inhibitory connections may be a key factor in the dissociation between local field potentials and spiking activity, which may contribute substantially to the close coupling between the BOLD signal and synchronized synaptic activity in the brain.

Studies are described which are intended to improve our understanding of the primary measurements made in non-invasive neural imaging. The blood oxygenation level-dependent signal used in functional magnetic resonance imaging (fMRI) reflects changes in deoxygenated haemoglobin. Tissue oxygen concentration, along with blood flow, changes during neural activation. Therefore, measurements of tissue oxygen together with the use of a neural sensor can provide direct estimates of neural–metabolic interactions. We have used this relationship in a series of studies in which a neural microelectrode is combined with an oxygen micro-sensor to make simultaneous co-localized measurements in the central visual pathway. Oxygen responses are typically biphasic with small initial dips followed by large secondary peaks during neural activation. By the use of established visual response characteristics, we have determined that the oxygen initial dip provides a better estimate of local neural function than the positive peak. This contrasts sharply with fMRI for which the initial dip is unreliable. To extend these studies, we have examined the relationship between the primary metabolic agents, glucose and lactate, and associated neural activity. For this work, we also use a Doppler technique to measure cerebral blood flow (CBF) together with neural activity. Results show consistent synchronously timed changes such that increases in neural activity are accompanied by decreases in glucose and simultaneous increases in lactate. Measurements of CBF show clear delays with respect to neural response. This is consistent with a slight delay in blood flow with respect to oxygen delivery during neural activation. This article is part of the themed issue ‘Interpreting BOLD: a dialogue between cognitive and cellular neuroscience’.

Neurons in the visual cortex are generally selective to direction of movement of a stimulus. Although models of this direction selectivity (DS) assume linearity, experimental data show stronger degrees of DS than those predicted by linear models. Our current study was intended to determine the degree of non-linearity of the DS mechanism for cells within different laminae of the cat's primary visual cortex. To do this, we analysed cells in our database by using neurophysiological and histological approaches to quantify non-linear components of DS in four principal cortical laminae (layers 2/3, 4, 5, and 6). We used a DS index (DSI) to quantify degrees of DS in our sample. Our results showed laminar differences. In layer 4, the main thalamic input region, most neurons were of the simple type and showed high DSI values. For complex cells in layer 4, there was a broad distribution of DSI values. Similar features were observed in layer 2/3, but complex cells were dominant. In deeper layers (5 and 6), DSI value distributions were characterized by clear peaks at high values. Independently of specific lamina, high DSI values were accompanied by narrow orientation tuning widths. Differences in orientation tuning for non-preferred vs. preferred directions were smallest in layer 4 and largest in layer 6. These results are consistent with a non-linear process of intra-cortical inhibition that enhances DS by selective suppression of neuronal firing for non-preferred directions of stimulus motion in a lamina-dependent manner. Other potential mechanisms are also considered.

Noninvasive neural imaging has become an important tool in both applied and theoretical applications. The hemodynamic properties that are measured in functional magnetic resonance imaging (fMRI), for example, are generally used to infer neuronal characteristics. In an attempt to provide empirical data to connect the hemodynamic measurements with neural function, we have conducted previous studies in which neural activity and tissue oxygen metabolic functions are determined together in co-localized regions of the central visual pathway. A basic question in this procedure is whether oxygen responses are coupled linearly in space and time with neural activity. We have previously examined temporal factors, and in the current study, spatial characteristics are addressed. We have recorded from neurons in the lateral geniculate nucleus (LGN) and striate cortex in anesthetized cats. In both structures, there is a classical receptive field (CRF) within which a neuron can be activated. There is also a region outside the CRF from which stimulation cannot activate the cell directly but can influence the response elicited from the CRF. In this investigation we have used several specific spatial stimulus patterns presented to either the CRF or the surrounding region or to both areas together in order to determine spatial response patterns. Within the CRF, we find that neural and metabolic responses sum in a nonlinear fashion but changes in these two measurements are closely coupled. For stimuli that extend beyond the CRF, neural activity is generally reduced while oxygen response exhibits uncoupled changes.

Orientation selectivity and its development are basic features of visual cortex. The original model of orientation selectivity proposes that elongated simple cell receptive fields are constructed from convergent input of an array of lateral geniculate nucleus neurons. However, orientation selectivity of simple cells in the visual cortex is generally greater than the linear contributions based on projections from spatial receptive field profiles. This implies that additional selectivity may arise from intracortical mechanisms. The hierarchical processing idea implies mainly linear connections, whereas cortical contributions are generally considered to be nonlinear. We have explored development of orientation selectivity in visual cortex with a focus on linear and nonlinear factors in a population of anesthetized 4-wk postnatal kittens and adult cats. Linear contributions are estimated from receptive field maps by which orientation tuning curves are generated and bandwidth is quantified. Nonlinear components are estimated as the magnitude of the power function relationship between responses measured from drifting sinusoidal gratings and those predicted from the spatial receptive field. Measured bandwidths for kittens are slightly larger than those in adults, whereas predicted bandwidths are substantially broader. These results suggest that relatively strong nonlinearities in early postnatal stages are substantially involved in the development of orientation tuning in visual cortex.

Neurons in visual cortex exhibit two major types of stimulus elicited suppression. One, cross-orientation suppression, occurs within the classical receptive field (CRF) when an orthogonal grating is superposed on one at optimal orientation. The second, surround suppression, occurs when the size of an optimally oriented grating extends beyond the CRF. Previous proposals suggest that intracortical inhibition is responsible for surround suppression whereas feedforward processes may underlie cross-orientation suppression. To gain more insight concerning these types of suppression, we have included measurements of metabolic function in addition to neural responses. We made co-localized measurements of multiple unit neural activity and tissue oxygen concentrations in the striate cortex of anaesthetized cats while using visual stimuli to activate the two kinds of suppression. Results show that the amplitude of the initial negative oxygen response increases with stimulus size but neural responses decrease as size extends beyond the CRF. This shows that oxygen consumption increases with stimulus size regardless of reduced neural response. On the other hand, amplitudes of both the initial negative oxygen component and the neural responses are simultaneously attenuated by the orthogonal mask in cross-orientation suppression. These different neurometabolic response patterns are consistent with suggestions that the two types of suppressive processes arise from different neural mechanisms.

SummaryElectrical brain stimulation is a promising tool for both experimental and clinical applications. However, the effects of stimulation on neuronal activity are highly variable and poorly understood. To investigate the basis of this variability, we performed extracellular recordings in the visual cortex following application of transcranial magnetic stimulation (TMS). Our measurements of spiking and local field potential activity exhibit two types of response patterns which are characterized by the presence or absence of spontaneous discharge following stimulation. This variability can be partially explained by state-dependent effects, in which higher pre-TMS activity predicts larger post-TMS responses. These results reveal the possibility that variability in the neural response to TMS can be exploited to optimize the effects of stimulation. It is conceivable that this feature could be utilized in real time during the treatment of clinical disorders.

The firing rates of neurons in the central visual pathway vary with stimulus strength, but not necessarily in a linear manner. In the contrast domain, the neural response function for cells in the primary visual cortex is characterized by expansive and compressive nonlinearities at low and high contrasts, respectively. A compressive nonlinearity at high contrast is also found for early visual pathway neurons in the lateral geniculate nucleus (LGN). This mechanism affects processing in the visual cortex. A fundamentally related issue is the possibility of an expansive nonlinearity at low contrast in LGN. To examine this possibility, we have obtained contrast–response data for a population of LGN neurons. We find for most cells that the best-fit function requires an expansive component. Additionally, we have measured the responses of LGN neurons to m-sequence white noise and examined the static relationship between a linear prediction and actual spike rate. We find that this static relationship is well fit by an expansive nonlinear power law with average exponent of 1.58. These results demonstrate that neurons in early visual pathways exhibit expansive nonlinear responses at low contrasts. Although this thalamic expansive nonlinearity has been largely ignored in models of early visual processing, it may have important consequences because it potentially affects the interpretation of a variety of visual functions.

Transcranial magnetic stimulation (TMS) is an increasingly common technique used to selectively modify neural processing. However, application of TMS is limited by uncertainty concerning its physiological effects. We applied TMS to the cat visual cortex and evaluated the neural and hemodynamic consequences. Short TMS pulse trains elicited initial activation (∼1 minute) and prolonged suppression (5 to 10 minutes) of neural responses. Furthermore, TMS disrupted the temporal structure of activity by altering phase relationships between neural signals. Despite the complexity of this response, neural changes were faithfully reflected in hemodynamic signals; quantitative coupling was present over a range of stimulation parameters. These results demonstrate long-lasting neural responses to TMS and support the use of hemodynamic-based neuroimaging to effectively monitor these changes over time.

The relationships between neural and metabolic processes in activated brain regions are central to the interpretation of noninvasive imaging. To examine this relationship, we have used a specialized sensor to measure simultaneously tissue oxygen changes and neural activity in colocalized regions of the cat's lateral geniculate nucleus (LGN). Previous work with this sensor has shown that a decrease or increase in tissue oxygen can be elicited by selective control of the location and extent of neural activation in the LGN. In the current study, to evaluate the temporal integration and homogeneity of neurometabolic coupling, we have determined the relationship between multiunit extracellular neural activity and tissue oxygen responses to visual stimuli of various durations and contrasts. Our results show that the negative but not the positive oxygen response changes in an approximately linear manner with stimulus duration. The relationship between the negative oxygen response and neural activity is relatively constant with stimulus duration. Moreover, both negative and positive oxygen responses saturate at high stimulus contrast levels. Coupling between neural activity and negative oxygen responses is well described by a power law function. These results help elucidate differences between the initial negative and subsequent positive metabolic responses and may be directly relevant to questions concerning brain mapping with functional magnetic resonance imaging.

In noninvasive neuroimaging, neural activity is inferred from local fluctuations in deoxyhemoglobin. A fundamental question of functional magnetic resonance imaging (fMRI) is whether the inferred neural activity is driven primarily by synaptic or spiking activity. The answer is critical for the interpretation of the blood oxygen level-dependent (BOLD) signal in fMRI. Here, we have used well-established visual-system circuitry to create a stimulus that elicits synaptic activity without associated spike discharge. In colocalized recordings of neural and metabolic activity in cat primary visual cortex, we observed strong coupling between local field potentials (LFPs) and changes in tissue oxygen concentration in the absence of spikes. These results imply that the BOLD signal is more closely coupled to synaptic activity.

Background Transcranial magnetic stimulation (TMS) is used to selectively alter neuronal activity of specific regions in the cerebral cortex. TMS is reported to induce either transient disruption or enhancement of different neural functions. However, its effects on tuning properties of sensory neurons have not been studied quantitatively. Objective/hypothesis Here, we use specific TMS application parameters to determine how they may alter tuning characteristics (orientation, spatial frequency, and contrast sensitivity) of single neurons in the cat's visual cortex. Methods Single unit spikes were recorded with tungsten microelectrodes from the visual cortex of anesthetized and paralyzed cats (12 males). Repetitive TMS (4 Hz, 4 s) was delivered with a 70 mm figure-8 coil. We quantified basic tuning parameters of individual neurons for each pre- and post-TMS condition. The statistical significance of changes for each tuning parameter between the two conditions was evaluated with a Wilcoxon signed-rank test. Results We generally find long-lasting suppression which persists well beyond the stimulation period. Pre- and post-TMS orientation tuning curves show constant peak values. However, strong suppression at non-preferred orientations tends to narrow the widths of tuning curves. Spatial frequency tuning exhibits an asymmetric change in overall shape, which results in an emphasis on higher frequencies. Contrast tuning curves show nonlinear changes consistent with a gain control mechanism. Conclusions These findings suggest that TMS causes extended interruption of the balance between sub-cortical and intra-cortical inputs.

A variety of studies in the visual system demonstrate that coarse spatial features are processed before those of fine detail. This aspect of visual processing is assumed to originate in striate cortex, where single cells exhibit a refinement of spatial frequency tuning over the duration of their response. However, in early visual pathways, well known temporal differences are present between center and surround components of receptive fields. Specifically, response latency of the receptive field center is relatively shorter than that of the surround. This spatiotemporal inseparability could provide the basis of coarse-to-fine dynamics in early and subsequent visual areas. We have investigated this possibility with three separate approaches. First, we predict spatial-frequency tuning dynamics from the spatiotemporal receptive fields of 118 cells in the lateral geniculate nucleus (LGN). Second, we compare these linear predictions to measurements of tuning dynamics obtained with a subspace reverse correlation technique. We find that tuning evolves dramatically in thalamic cells, and that tuning changes are generally consistent with the temporal differences between spatiotemporal receptive field components. Third, we use a model to examine how different sources of dynamic input from early visual pathways can affect tuning in cortical cells. We identify two mechanisms capable of producing substantial dynamics at the cortical level: (1) the center-surround delay in individual LGN neurons, and (2) convergent input from multiple cells with different receptive field sizes and response latencies. Overall, our simulations suggest that coarse-to-fine tuning in the visual cortex can be generated completely by a feedforward process.

The response of a neuron in striate cortex to an optimally oriented stimulus is suppressed by a superimposed orthogonal stimulus. The neural mechanism underlying this cross-orientation suppression (COS) may arise from intracortical or subcortical processes or from both. Recent studies of the temporal frequency and adaptation properties of COS suggest that depression at thalamo-cortical synapses may be the principal mechanism. To examine the possible role of synaptic depression in relation to COS, we measured the recovery time course of COS. We find it too rapid to be explained by synaptic depression. We also studied potential subcortical processes by measuring single cell contrast response functions for a population of LGN neurons. In general, contrast saturation is a consistent property of LGN neurons. Combined with rectifying nonlinearities in the LGN and spike threshold nonlinearities in visual cortex, contrast saturation in the LGN can account for most of the COS that is observed in the visual cortex.

Various properties of external scenes are integrated during the transmission of information along central visual pathways. One basic property concerns the sensitivity to direction of a moving stimulus. This direction selectivity (DS) is a fundamental response characteristic of neurons in the visual cortex. We have conducted a neurophysiological study of cells in the visual cortex to determine how DS is affected by changes in stimulus contrast. Previous work shows that a neuron integration time is increased at low contrasts, causing temporal changes of response properties. This leads to the prediction that DS should change with stimulus contrast. However, the change could be in a counterintuitive direction, i.e., DS could increase with reduced contrast. This possibility is of intrinsic interest but it is also of potential relevance to recent behavioral work in which human subjects exhibit increased DS as contrast is reduced. Our neurophysiological results are consistent with this finding, i.e., the degree of DS of cortical neurons is inversely related to stimulus contrast. Temporal phase differences of inputs to cortical cells may account for this result.

Neural activity is closely coupled with energy metabolism but details of the association remain to be identified. One basic area involves the relationships between neural activity and the main supportive substrates of glucose and lactate. This is of fundamental significance for the interpretation of non-invasive neural imaging. Here, we use microelectrodes with high spatial and temporal resolution to determine simultaneous co-localized changes in glucose, lactate, and neural activity during visual activation of the cerebral cortex in the cat. Tissue glucose and lactate concentration levels are measured with electrochemical microelectrodes while neural spiking activity and local field potentials are sampled by a microelectrode. These measurements are performed simultaneously while neurons are activated by visual stimuli of different contrast levels, orientations, and sizes. We find immediate decreases in tissue glucose concentration and simultaneous increases in lactate during neural activation. Both glucose and lactate signals return to their baseline levels instantly as neurons cease firing. No sustained changes or initial dips in glucose or lactate signals are elicited by visual stimulation. However, co-localized measurements of cerebral blood flow and neural activity demonstrate a clear delay in the cerebral blood flow signal such that it does not correlate temporally with the neural response. These results provide direct real-time evidence regarding the coupling between co-localized energy metabolism and neural activity during physiological stimulation. They are also relevant to a current question regarding the role of lactate in energy metabolism in the brain during neural activation. Dynamic changes in energy metabolites can be measured directly with high spatial and temporal resolution by use of enzyme-based microelectrodes. Here, to examine neuro-metabolic coupling during brain activation, we use combined microelectrodes to simultaneously measure extracellular glucose, lactate, and neural responses in the primary visual cortex to visual stimulation. We demonstrate rapid decreases in glucose and increases in lactate during neural activation. Changes in glucose and lactate signals are transient and closely coupled with neuronal firing.

For binocular animals viewing a three-dimensional scene, the left and right eyes receive slightly different information, and the brain uses this 'binocular disparity' to interpret stereoscopic depth. An important theoretical conjecture in this mechanism is that coarse processing precedes and constrains finely detailed processing. We present three types of neurophysiological data from the cat's visual cortex that are consistent with a temporal coarse-to-fine tuning of disparity information. First, the disparity tuning of cortical cells generally sharpened during the time course of response. Second, cells responsive to large and small spatial scale had relatively shorter and longer temporal latencies, respectively. Third, cross-correlation analysis between simultaneously recorded pairs of cortical cells showed that connections between disparity-tuned neurons were generally stronger for coarse-to-fine processing than for fine-to-coarse processing. These results are consistent with theoretical and behavioral studies and suggest that rapid, coarse percepts are refined over time in stereoscopic depth perception.

Organization of the central visual pathway is generally studied from a perspective of feedforward processes. However, there are horizontal connections and also strong feedback from extra striate to visual cortex. Here, we use visual stimuli designed to maximize relative differential involvements of these three main types of connections. The approach relies on differences between stimulation within the classical receptive field (CRF) and that of the surround region. Although previous studies have used similar approaches, they were limited primarily to spatial segregation of neural connections. Our experimental design provides clear segregation of fast and slow components of surround modulation. We assume these are mediated by feedback and horizontal connections, respectively, but other factors may be involved. Our results imply that both horizontal and feedback connections contribute to integration of visual information outside the CRF and provide suppressive or facilitative modulation. For a given cell, modulation may change in strength and sign from suppression to facilitation or the reverse depending on surround parameters. Sub-threshold input from the CRF surround increases local field potential (LFP) power in distinct frequency ranges which differ for suppression and facilitation. Horizontal connections have delayed CRF-surround modulation and are sensitive to position changes in the surround. Therefore, surround information beyond the CRF is initially processed by fast connections which we consider to be feedback, whereas spatially tuned mechanisms are relatively slow and presumably mediated by horizontal connections. Overall, results suggest that convergent fast (feedforward) inputs determine size and structure of the CRFs of recipient cells in visual cortex. And fast connections from extra striate regions (feedback) plus slow-tuned connections (horizontal) within visual cortex contribute to spatial influences of CRF surround activation.

At reduced luminance levels, the visual system integrates light over extended periods of time. Although the general effects of this process are known, specific changes in the visual cortex have not been identified. We have studied the physiological changes that occur during a transition from high to low luminance by measurements of single neurons in the cat's primary visual cortex. Under low-luminance conditions, we find increased latencies, expanded temporal responses, and a loss of temporal structure. This results in temporal-frequency tuning curves that are peaked at relatively low frequencies. To examine parallel perceptual changes, we compared perceived temporal frequency in human subjects under high- and low-luminance conditions. Low-luminance flickering patterns are perceived to modulate at relatively high rates. This occurs even though peak sensitivity is shifted to relatively low temporal frequencies. To explore further the perceptual component, we measured perceived temporal frequency in human subjects with unilateral optic neuritis for whom optic nerve transmission is known to be relatively slow and generally similar to the normal physiological state under low luminance. These subjects also perceive relatively high modulation rates through their affected eye. Considered together, these results demonstrate an inverse relationship between the physiological and the perceptual consequences of reduced stimulus luminance. This relationship may be accounted for by shifts of neuronal population responses between high- and low-luminance levels.

The important visual stimulus parameters for a given cell are defined by the classical receptive field (CRF). However, cells are also influenced by visual stimuli presented in areas surrounding the CRF. The experiments described here were conducted to determine the incidence and nature of CRF surround influences in the primary visual cortex. From extracellular recordings in the cat's striate cortex, we find that for over half of the cells investigated (56%, 153/271), the effect of stimulation in the surround of the CRF is to suppress the neuron's activity by at least 10% compared to the response to a grating presented within the CRF alone. For the remainder of the cells, the interactions were minimal and a few were of a facilitatory nature. In this paper, we focus on the suppressive interactions. Simple and complex cell types exhibit equal incidences of surround suppression. Suppression is observed for cells in all layers, and its degree is strongly correlated between the two eyes for binocular neurons. These results show that surround suppression is a prevalent form of inhibition and may play an important role in visual processing.

In this study, we compare binocular and monocular mechanisms underlying contrast encoding by binocular simple cells in primary visual cortex. At mid to high levels of stimulus contrast, contrast gain of cortical neurons typically decreases as stimulus contrast is increased (Albrecht and Hamilton, 1982). We have devised a technique by which it is possible to determine the relative contributions of monocular and binocular processes to such reductions in contrast gain. First, we model the simple cell as an adjustable linear mechanism with a static output nonlinearity. For binocular cells, the linear mechanism is sensitive to inputs from both eyes. To constrain the parameters of the model, we record from binocular simple cells in striate cortex. To activate each cell, drifting sinusoidal gratings are presented dichoptically at various relative interocular phases. Stimulus contrast for one eye is varied over a large range whereas that for the other eye is fixed. We then determine the best-fitting parameters of the model for each cell for all of the interocular contrast ratios. This allows us to determine the effect of contrast on the contrast gain of the system. Finally, we decompose the contrast gain into monocular and binocular components. Using the data to constrain the model for a fixed contrast in one eye and increased contrasts in the other eye, we find steep reductions in monocular gain, whereas binocular gain exhibits modest and variable changes. These findings demonstrate that contrast gain reductions occur primarily at a monocular site, before convergence of information from the two eyes.

Areas beyond the classical receptive field (CRF) can modulate responses of the majority of cells in the primary visual cortex of the cat (Walker et al., 1999). Although general characteristics of this phenomenon have been reported previously, little is known about the detailed spatial organization of the surrounds. Previous work suggests that the surrounds may be uniform regions that encircle the CRF or may be limited to the “ends” of the CRF. We have examined the spatial organization of surrounds of single-cell receptive fields in the primary visual cortex of anesthetized, paralyzed cats. The CRF was stimulated with an optimal drifting grating, whereas the surround was probed with a second small grating patch placed at discrete locations around the CRF. For most cells that exhibit suppression, the surrounds are spatially asymmetric, such that the suppression originates from a localized region. We find a variety of suppressive zone locations, but there is a slight bias for suppression to occur at the end zones of the CRF. The spatial pattern of suppression is independent of the parameters of the suppressive stimulus used, although the effect is clearest with iso-oriented surround stimuli. A subset of cells exhibit axially symmetric or uniform surround fields. These results demonstrate that the surrounds are more specific than previously realized, and this specialization has implications for the processing of visual information in the primary visual cortex. One possibility is that these localized surrounds may provide a substrate for figure–ground segmentation of visual scenes.

Orientation selectivity is one of the most conspicuous receptive-field (RF) properties that distinguishes neurons in the striate cortex from those in the lateral geniculate nucleus (LGN). It has been suggested that orientation selectivity arises from an elongated array of feedforward LGN inputs (Hubel & Wiesel, 1962). Others have argued that cortical mechanisms underlie orientation selectivity (e.g. Sillito, 1975; Somers et al., 1995). However, isolation of each mechanism is experimentally difficult and no single study has analyzed both processes simultaneously to address their relative roles. An alternative approach, which we have employed in this study, is to examine the relative contributions of linear and nonlinear mechanisms in sharpening orientation tuning. Since the input stage of simple cells is remarkably linear, the nonlinear contribution can be attributed solely to cortical factors. Therefore, if the nonlinear component is substantial compared to the linear contribution, it can be concluded that cortical factors play a prominent role in sharpening orientation tuning. To obtain the linear contribution, we first measure RF profiles of simple cells in the cat's striate cortex using a binary m-sequence noise stimulus. Then, based on linear spatial summation of the RF profile, we obtain a predicted orientation-tuning curve, which represents the linear contribution. The nonlinear contribution is estimated as the difference between the predicted tuning curve and that measured with drifting sinusoidal gratings. We find that measured tuning curves are generally more sharply tuned for orientation than predicted curves, which indicates that the linear mechanism is not enough to account for the sharpness of orientation-tuning. Therefore, cortical factors must play an important role in sharpening orientation tuning of simple cells. We also examine the relationship of RF shape (subregion aspect ratio) and size (subregion length and width) to orientation-tuning halfwidth. As expected, predicted tuning halfwidths are found to depend strongly on both subregion length and subregion aspect ratio. However, we find that measured tuning halfwidths show only a weak correlation with subregion aspect ratio, and no significant correlation with RF length and width. These results suggest that cortical mechanisms not only serve to sharpen orientation tuning, but also serve to make orientation tuning less dependent on the size and shape of the RF. This ensures that orientation is represented equally well regardless of RF size and shape.

The visual system integrates information from the left and right eyes and constructs a visual world that is perceived as single and three dimensional. To understand neural mechanisms underlying this process, it is important to learn about how signals from the two eyes interact at the level of single neurons. Using a sophisticated receptive field (RF) mapping technique that employs binary m-sequences, we have determined the rules of binocular interactions exhibited by simple cells in the cat’s striate cortex in relation to the structure of their monocular RFs. We find that binocular interaction RFs of most simple cells are well described as the product of left and right eye RFs. Therefore the binocular interactions depend not only on binocular disparity but also on monocular stimulus position or phase. The binocular interaction RF is consistent with that predicted by a model of a linear binocular filter followed by a static nonlinearity. The static nonlinearity is shown to have a shape of a half-power function with an average exponent of ∼2. Although the initial binocular convergence of signals is linear, the static nonlinearity makes binocular interaction multiplicative at the output of simple cells. This multiplicative binocular interaction is a key ingredient for the computation of interocular cross-correlation, an algorithm for solving the stereo correspondence problem. Therefore simple cells may perform initial computations necessary to solve this problem.

It is well established that multiple stimulus dimensions (e.g., orientation and spatial frequency) are mapped onto the surface of striate cortex. However, the detailed organization of neurons within a local region of striate cortex remains unclear. Within a vertical column, do all neurons have the same response selectivities? And if not, how do they most commonly differ and why? To address these questions, we recorded from nearby pairs of simple cells and made detailed spatiotemporal maps of their receptive fields. From these maps, we extracted and analyzed a variety of response metrics. Our results provide new insights into the local organization of striate cortex. First, we show that nearby neurons seldom have very similar receptive fields, when these fields are characterized in space and time. Thus, there may be less redundancy within a column than previously thought. Moreover, we show that correlated discharge increases with receptive field similarity; thus, the local dissimilarity between neurons may allow for noise reduction by response pooling. Second, we show that several response variables are clustered within striate cortex, including some that have not received much attention such as response latency and temporal frequency. We also demonstrate that other parameters are not clustered, including the spatial phase (or symmetry) of the receptive field. Third, we show that spatial phase is the single parameter that accounts for most of the difference between receptive fields of nearby neurons. We consider the implications of this local diversity of spatial phase for population coding and construction of higher-order receptive fields.

Recent experiments have provided new clues as to how, in visual perception, three-dimensional depth is signaled and integrated with image motion.

Synchronized oscillatory discharge in the visual cortex has been proposed to underlie the linking of retinotopically disparate features into perceptually coherent objects. These proposals have largely relied on the premise that the oscillations arise from intracortical circuitry. However, strong oscillations within both the retina and the lateral geniculate nucleus (LGN) have been reported recently. To evaluate the possibility that cortical oscillations arise from peripheral pathways, we have developed two plausible models of single cell oscillatory discharge that specifically exclude intracortical networks. In the first model, cortical oscillatory discharge near 50 Hz in frequency arises from the integration of signals from strongly oscillatory cells within the LGN. The model also predicts the incidence of 50-Hz oscillatory cells within the cortex. Oscillatory discharge around 30 Hz is explained in a second model by the presence of intrinsically oscillatory cells within cortical layer 5. Both models generate spike trains whose power spectra and mean firing rates are in close agreement with experimental observations of simple and complex cells. Considered together, the two models can largely account for the nature and incidence of oscillatory discharge in the cat's visual cortex. The validity of these models is consistent with the possibility that oscillations are generated independently of intracortical interactions. Because these models rely on intrinsic stimulus-independent oscillators within the retina and cortex, the results further suggest that oscillatory activity within the cortex is not necessarily associated with the processing of high-order visual information.

Cai, Daqing, Gregory C. DeAngelis, and Ralph D. Freeman. Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. J. Neurophysiol. 78: 1045–1061, 1997. We have studied the spatiotemporal receptive-field organization of 144 neurons recorded from the dorsal lateral geniculate nucleus (dLGN) of adult cats and kittens at 4 and 8 wk postnatal. Receptive-field profiles were obtained with the use of a reverse correlation technique, in which we compute the cross-correlation between the action potential train of a neuron and a randomized sequence of long bright and dark bar stimuli that are flashed throughout the receptive field. Spatiotemporal receptive-field profiles of LGN neurons generally exhibit a biphasic temporal response, as well as the classical center-surround spatial organization. For nonlagged cells, the first temporal phase of the response dominates, whereas for lagged neurons, the second temporal phase of the response is typically the largest. This temporal phase difference between lagged and nonlagged cells accounts for their divergent behavior in response to flashed stimuli. Most LGN cells exhibit some degree of space-time inseparability, which means that the receptive field cannot simply be viewed as the product of a spatial waveform and a temporal waveform. In these cases, the response of the surround is typically delayed relative to that of the center, and there is some blending of center and surround during the time course of the response. We demonstrate that a simple extension of the traditional difference-of-Gaussians (DOG) model, in which the surround response is delayed relative to that of the center, accounts nicely for these findings. With regard to development, our analysis shows that spatial and temporal aspects of receptive field structure mature with markedly different time courses. After 4 wk postnatal, there is little change in the spatial organization of LGN receptive fields, with the exception of a weak, but significant, trend for the surround to become smaller and stronger with age. In contrast, there are substantial changes in temporal receptive-field structure after 4 wk postnatal. From 4 to 8 wk postnatal, the shape of the temporal response profile changes, becoming more biphasic, but the latency and duration of the response remain unchanged. From 8 wk postnatal to adulthood, the shape of the temporal profile remains approximately constant, but there is a dramatic decline in both the latency and duration of the response. Comparison of our results with recent data from cortical (area 17) simple cells reveals that the temporal development of LGN cells accounts for a substantial portion of the temporal maturation of simple cells.

The spatial components of a visual scene are processed neurally in a sequence of coarse features followed by fine features. This coarse-to-fine temporal stream was initially considered to be a cortical function, but has recently been demonstrated in the dorsal lateral geniculate nucleus. The goal of this study was to test the hypothesis that coarse-to-fine processing is present at earlier stages of visual processing in the retinal ganglion cells that supply lateral geniculate nucleus (LGN) neurons. To compare coarse-to-fine processing in the cat's visual system, we measured the visual responses of connected neuronal pairs from the retina and LGN, and separate populations of cells from each region. We found that coarse-to-fine processing was clearly present at the ganglion cell layer of the retina. Interestingly, peak and high-spatial-frequency cutoff responses were higher in the LGN than in the retina, indicating that there was a progressive cascade of coarse-to-fine information from the retina to the LGN to the visual cortex. The analysis of early visual pathway receptive field characteristics showed that the physiological response interplay between the center and surround regions was consistent with coarse-to-fine features and may provide a primary role in the underlying mechanism. Taken together, the results from this study provided a framework for understanding the emergence and refinement of coarse-to-fine processing in the visual system.

The objective of this study was to evaluate the maturity of three inhibitory mechanisms (end-inhibition, side-inhibition, and cross-orientation inhibition) in the striate cortex of kittens at 4 weeks postnatal. To accomplish this, we made extracellular recordings from area 17 neurons while presenting visual stimuli consisting of sinusoidal luminance gratings or composites of gratings. We then compared data from kittens relating to various characteristics of each inhibitory mechanism with data from adults. We find that end-inhibition, side-inhibition, and cross-orientation inhibition are all present in kittens, and all show signs of maturity by 4 weeks postnatal. We conclude that the development of these inhibitory mechanisms occurs relatively early, and may coincide with the development of excitatory properties.

Neurons in the central visual pathways process visual images within a localized region of space, and a restricted epoch of time. Although the receptive field (RF) of a visually responsive neuron is inherently a spatiotemporal entity, most studies have focused exclusively on spatial aspects of RF structure. Recently, however, the application of sophisticated RF-mapping techniques has enabled neurophysiologists to characterize RFs in the joint domain of space and time. Studies that use these techniques have revealed that neurons in the geniculostriate pathway exhibit striking RF dynamics. For a majority of cells, the spatial structure of the RF changes as a function of time; thus, these RFs can be characterized adequately only in the space-time domain. In this review, the spatiotemporal RF structure of neurons in the lateral geniculate nucleus and primary visual cortex is discussed.

Binocular neurons in the visual cortex are thought to form the neural substrate for stereoscopic depth perception. How are the receptive fields of these binocular neurons organized to encode the retinal position disparities that arise from binocular parallax? The conventional notion is that the two receptive fields of a binocular neuron have identical shapes, but are spatially offset from the point of retinal correspondence (zero disparity). We consider an alternative disparity-encoding scheme, in which the two receptive fields may differ in shape (or phase), but are centered at corresponding retinal locations. Using a reverse-correlation technique to obtain detailed spatiotemporal receptive-field maps, we provide support for the latter scheme. Specifically, we show that receptive-field profiles for the left and right eyes are matched for cells that are tuned to horizontal orientations of image contours. However, for neurons tuned to vertical orientations, the left and right receptive fields are predominantly dissimilar in shape. These results show that the striate cortex possesses a specialized mechanism for processing vertical contours, which carry the horizontal–disparity information needed for stereopsis. Thus, in a major modification to the traditional notion of the neural basis of stereopsis, we propose that binocular simple cells encode horizontal disparities in terms of phase at multiple spatial scales. Implications of this scheme are discussed with respect to the size–disparity correlation observed in psychophysical studies.

Blood oxygen level–dependent functional magnetic resonance imaging uses alterations in brain hemodynamics to infer changes in neural activity. Are these hemodynamic changes regulated at a spatial scale capable of resolving functional columns within the cerebral cortex? To address this question, we made simultaneous measurements of tissue oxygenation and single-cell neural activity within the visual cortex. Results showed that increases in neuronal spike rate were accompanied by immediate decreases in tissue oxygenation. We used this decrease in tissue oxygenation to predict the orientation selectivity and ocular dominance of neighboring neurons. Our results establish a coupling between neural activity and oxidative metabolism and suggest that high-resolution functional magnetic resonance imaging may be used to localize neural activity at a columnar level.

Columnar structure in the cerebral cortex has been demonstrated in numerous studies. However, in the visual system, it is not clear from imaging, basic physiological and anatomical approaches how multiple stimulus parameters are related within columns. We have analyzed recordings from pairs of neurons in the striate cortex of the cat using various spatial and temporal parameters. We find that most parameters are clustered within inferred columns with the exception of spatial phase. Diversity of phase could be useful for serial processing in central visual pathways.

1. To investigate the functional significance of temporally correlated discharge between nearby cells in the visual cortex, we obtained receptive-field maps of correlated discharge for 68 cell pairs in kittens and cats. Discharge from cell pairs was measured by a single extracellular electrode. A reverse correlation procedure was used to relate neural discharge to particular stimuli within a random sequence of briefly flashed bright and dark bars. Bicellular receptive fields (BRFs) were mapped by applying reverse correlation to approximately synchronous discharge from two cells. Unicellular receptive fields (URFs) were simultaneously mapped by separately applying reverse correlation to the discharge of each cell. 2. The receptive fields of the two neurons within each pair were initially studied by varying the orientation and spatial frequency of drifting sinusoidal gratings. After these tests a random sequence of appropriately oriented bars was used to evoke discharge suitable for reverse correlation analysis. For most cell pairs, the temporal pattern or strength of correlated discharge produced by such stimulation is different from that observed with stimulation by sinusoidal gratings. This indicates that visually evoked correlated discharge between nearby cells is stimulus dependent. 3. BRFs were classified according to their pattern of spatial sensitivity into three groups that roughly correspond to the single-cell receptive-field types of the lateral geniculate nucleus (LGN; center-surround) and visual cortex (simple and complex). These classifications were compared with the receptive-field types of the single cells within each pair. LGN-type and simple-type BRFs were only seen for pairs in which at least one of the cells was simple. Conversely, complex-type BRFs were only seen for pairs in which at least one of the cells was complex. 4. Because the reverse correlation procedure can be used to characterize the spatiotemporal receptive-field structure of simple cells, we were able to compare both the spatial and temporal properties associated with the URFs and BRFs of simple cell pairs. The spatiotemporal structure of the BRF of a simple-cell pair can largely be predicted on the basis of the two URFs. Although this prediction suggests the possibility that BRFs are stimulus artifacts, a shuffle procedure, in which multiple repetitions of random sequences were presented, verifies the neural origin of BRFs. BRFs emerge from specific neural pathways and are not simply a consequence of unicellular response preferences. 5. Five measures were derived from the reverse correlation analysis of simple-cell receptive fields: width, duration, optimal spatial and temporal frequency, and optimal velocity.(ABSTRACT TRUNCATED AT 400 WORDS)

Exposure to specific visual stimuli causes a reduction in sensitivity to similar subsequent stimulation. This adaptation effect is observed behaviorally and for neurons in the primary visual cortex. Here, we explore the effects of adaptation on neurons that encode binocular depth discrimination in the cat's primary visual cortex. Our results show that neuronal preference for binocular depth is altered selectively with appropriate adaptation. At the preferred depth, adaptation causes substantial suppression of subsequent responses. Near the preferred depth, the same procedure causes a shift in depth preference. At the null depth, adaptation has little effect on binocular depth coding. These results demonstrate that prior exposure can change the depth selectivity of binocular neurons. The findings are relevant to the theoretical treatment of binocular depth processing. Specifically, the prevailing notion of binocular depth encoding based on the energy model requires modification.

1. We have tested the hypothesis that simple cells in the cat's visual cortex perform a linear spatiotemporal filtering of the visual image. To conduct this study we note that a visual neuron behaves linearly if the responses to small, brief flashes of light are mathematically related, via the Fourier transform, to the responses elicited by sinusoidal grating stimuli. 2. We have evaluated the linearity of temporal and spatial summation for 118 simple cells recorded from the striate cortex (area 17) of adult cats and kittens at ages 4 and 8 wk postnatal. These neurons represent a subset of the population of cells for which we have described the postnatal development of spatiotemporal receptive-field structure in the preceding paper. Spatiotemporal receptive-field profiles are constructed, with the use of a reverse correlation technique, from the responses to random sequences of small bar stimuli that are brighter or darker than the background. Fourier analysis of spatiotemporal receptive-field profiles yields linear predictions of the cells' spatial and temporal frequency tuning. These predicted responses are compared with spatial and temporal frequency tuning curves measured by the use of drifting, sinusoidal-luminance grating stimuli. 3. For most simple cells, there is good agreement between spatial and temporal frequency tuning curves predicted from the receptive-field profile and those measured by the use of sinusoidal gratings. These results suggest that both spatial and temporal summation within simple cells are approximately linear. There is a tendency for predicted tuning curves to be slightly broader than measured tuning curves, a finding that is consistent with the effects of a threshold nonlinearity at the output of these neurons. In some cases, however, predicted tuning curves deviate from measured responses only at low spatial and temporal frequencies. This cannot be explained by a simple threshold nonlinearity. 4. If linearity is assumed, it should be possible to predict the direction selectivity of simple cells from the structure of their spatiotemporal receptive-field profiles. For virtually all cells, linear predictions correctly determine the preferred direction of motion of a visual stimulus. However, the strength of the directional bias is typically underestimated by a factor of about two on the basis of linear predictions. Consideration of the expansive exponential nonlinearity revealed in the contrast-response function permits a reconciliation of the discrepancy between measured and predicted direction selectivity indexes. 5. Overall, these findings show that spatiotemporal receptive-field profiles obtained with the use of reverse correlation may be used to predict a variety of response properties for simple cells.(ABSTRACT TRUNCATED AT 400 WORDS)

1. Most studies of cortical neurons have focused on the spatial structure of receptive fields. For a more complete functional description of these neurons, it is necessary to consider receptive-field structure in the joint domain of space and time. We have studied the spatiotemporal receptive-field structure of 233 simple cells recorded from the striate cortex of adult cats and kittens at 4 and 8 wk postnatal. The dual goal of this study is to provide a detailed quantitative description of spatiotemporal receptive-field structure and to compare the developmental time courses of spatial and temporal response properties. 2. Spatiotemporal receptive-field profiles have been measured with the use of a reverse correlation method, in which we compute the cross-correlation between a neuron's response and a random sequence of small, briefly presented bright and dark stimuli. The receptive-field profiles of some simple cells are space-time separable, meaning that spatial and temporal response characteristics can be dissociated. Other cells have receptive-field profiles that are space-time inseparable. In these cases, a particular spatial location cannot be designated, unambiguously, as belonging to either an on or off subregion. However, separate on and off subregions may be clearly distinguished in the joint space-time domain. These subregions are generally tilted along an oblique axis. 3. Our observations show that spatial and temporal aspects of receptive-field structure mature with clearly different time courses. By 4 wk postnatal, the spatial symmetry and periodicity of simple-cell receptive fields have reached maturity. The spatial extent (or size) of these receptive fields is adult-like by 8 wk postnatal. In contrast, the response latency and time duration of spatiotemporal receptive fields do not mature until well beyond 8 wk postnatal. 4. By applying Fourier analysis to spatiotemporal receptive-field profiles, we have examined the postnatal development of spatial and temporal selectivity in the frequency domain. By 8 wk postnatal, spatial frequency tuning has clearly reached maturity. On the contrary, temporal frequency selectivity remains markedly immature at 8 wk. We have also examined the joint distribution of optimal spatial and temporal frequencies. From 4 wk postnatal until 8 wk postnatal, the range of optimal spatial frequencies increases substantially, whereas the range of optimal temporal frequencies remains largely unchanged. From 8 wk postnatal until adulthood, there is a large increase in optimal temporal frequencies for cells tuned to low spatial frequencies. For cells tuned to high spatial frequencies, the distribution of optimal temporal frequencies does not change much beyond 8 wk postnatal.(ABSTRACT TRUNCATED AT 400 WORDS)

Attempts have been made in various studies to identify and trace changes in function in the aging visual system. Some results are conflicting and we report here a unique approach in an attempt to resolve selected issues. We have estimated neurometabolic coupling in the central visual pathway in young and old cats. Our technique provides high resolution simultaneous measurements of neuronal activity and changes in concentration of tissue oxygen in the thalamus of young and old cats. Following visual stimulation, we find shorter latency and time to peak in tissue oxygen responses in old compared with young animals. Estimates of local activity induced initial negative oxygen response show substantial reductions in older animals. Measurements of neural activity in the form of multiple unit activity are similar in the two age groups. To investigate the mechanisms underlying the changes in tissue oxygen response in older animals, we measured vascular capillary density and found it to be substantially lower in old than that in young animals. Together, these findings suggest that the changes in metabolic responses with age may be largely accounted for by alterations in the cerebral microvasculature rather than by changes in neural activity.

1. The discharge of individual neurons in the visual cortex and lateral geniculate nucleus (LGN) of anesthetized and paralyzed cats and kittens was examined for the presence of oscillatory activity. Neural firing was evoked through the monoptic or dichoptic presentation of drifting gratings and random sequences of flashed bars. The degree to which different oscillatory frequencies were present in neural discharge was quantified by computation of the power spectra of impulse train responses. 2. Action potentials from single cells were recorded extracellularly and isolated on the basis of amplitude. Receptive-field properties of the neurons under study were characterized initially by their discharge in response to gratings of sinusoidal luminance. By varying orientation and spatial frequency, optimal stimulus characteristics were determined. Oscillation analysis was performed on spike trains acquired during repeated presentations of the optimal stimulus by identification of power spectra peaks in the frequency range of rhythmic potentials observed in electroencephalograph studies (30-80 Hz). The amplitude and frequency of the largest peak in this range was used to characterize oscillatory strength and frequency. All discharge in which the peak amplitude exceeded the high-frequency noise by a factor > 1.5 was classified as oscillatory. 3. Of the 342 cortical cells examined, 147 cells displayed oscillatory activity in the 30 to 80-Hz range during portions of their visual response. Sixty out of 169 simple cells, 82 out of 166 complex cells, and 5 out of 7 special complex cells exhibited oscillations. There was no laminar bias in the distribution of oscillatory cells; the proportions of oscillatory cells were similar in all layers. All oscillatory discharge was variable with respect to frequency and strength between successive presentations of the same optimal stimulus. In as little as 10 s, for example, peak frequencies shifted by a factor of two. For many cells, these trial-to-trial variations obscured detectable oscillations when all trials were averaged together. 4. The potential role of neuronal maturation in the generation of oscillatory activity was investigated by studying neuronal responses from kittens at 4 wk postnatal. Of the 80 kitten cells studied, 27 exhibited oscillatory discharge. Although oscillations in the kitten visual cortex spanned the same frequency range as that seen in the adult, oscillations in the midfrequency range (36-44 Hz) are more common in the adult cortex. 5. To explore the possibility that oscillations might play a functional role in vision, we investigated the dependence of oscillations on different stimulus parameters.(ABSTRACT TRUNCATED AT 400 WORDS)

The considerable mixing in the visual cortex, of signals from left and right eyes, provides an abundant population of binocularly activated neurons. Based on this and on the fact that cortical cells respond best to different ranges of retinal disparities, it has been proposed that these neurons form the physiological substrate of stereoscopic depth discrimination. We outline reasons here for addressing first the more fundamental issue of the rules of convergence in the visual cortex, for input from the two eyes. We show that most of this convergence may be described by a linear summation process. However, there is a nonlinear mechanism that maintains binocular interaction regardless of large differences in stimulus strength between the eyes. This finding suggests that a cell which appears to be dominated by one eye, when monocular tests are conducted, may respond equally under binocular conditions. In this case, binocular processing for all cortical cells could be uniform and independent of the ocular dominance values determined monocularly. With respect to a neural mechanism for the processing of information concerning different depths in space, we propose an alternative to the conventional notion. First, we identify fundamental problems with the current view. Second, we describe a procedure which allows us to distinguish between the conventional view and our alternative proposal. Standard receptive field mapping techniques are not adequate for determining phase-disparity relationships of the type we require. Therefore, we have employed a reverse correlation procedure which enables efficient and detailed mapping of receptive field structure. Third, we describe preliminary data concerning the physiological mechanism of stereoscopic depth discrimination.

Adaptation to a high-contrast grating stimulus causes reduced sensitivity to subsequent presentation of a visual stimulus with similar spatial characteristics. This behavioral finding has been attributed by neurophysiological studies to processes within the visual cortex. However, some evidence indicates that contrast adaptation phenomena are also found in early visual pathways. Adaptation effects have been reported in retina and lateral geniculation nucleus (LGN). It is possible that these early pathways could be the physiological origin of the cortical adaptation effect. To study this, we recorded from single neurons in the cat's LGN. We find that contrast adaptation in the LGN, unlike that in the visual cortex, is not spatial frequency specific, i.e., adaptation effects apply to a broad range of spatial frequencies. In addition, aside from the amplitude attenuation, the shape of spatial frequency tuning curves of LGN cells is not affected by contrast adaptation. Again, these findings are unlike those found for cells in the visual cortex. Together, these results demonstrate that pattern specific contrast adaptation is a cortical process.

The relationship between oxygen levels and neural activity in the brain is fundamental to functional neuroimaging techniques. We have examined this relationship on a fine spatial scale in the lateral geniculate nucleus (LGN) and visual cortex of the cat using a microelectrode sensor that provides simultaneous colocalized measurements of oxygen partial pressure in tissue (tissue oxygen) and multiunit neural activity. In previous work with this sensor, we found that changes in tissue oxygen depend strongly on the location and spatial extent of neural activation. Specifically, focal neural activity near the microelectrode elicited decreases in tissue oxygen, whereas spatially extended activation, outside the field of view of our sensor, yielded mainly increases. In the current study, we report an expanded set of measurements to quantify the spatiotemporal relationship between neural responses and changes in tissue oxygen. For the purpose of data analysis, we develop a quantitative model that assumes that changes in tissue oxygen are composed of two response components (one positive and one negative) with magnitudes determined by neural activity on separate spatial scales. Our measurements from visual cortex and the LGN are consistent with this model and suggest that the positive response spreads over a distance of 1–2 mm, whereas the negative component is confined to a few hundred micrometers. These results are directly relevant to the mechanisms that generate functional brain imaging signals and place limits on their spatial properties.

The response of a cell in the primary visual cortex to an optimally oriented grating is suppressed by a superimposed orthogonal grating. This cross-orientation suppression (COS) is exhibited when the orthogonal and optimal stimuli are presented to the same eye (monoptically) or to different eyes (dichoptically). A recent study suggested that monoptic COS arises from subcortical processes; however, the mechanisms underlying dichoptic COS were not addressed. We have compared the temporal frequency tuning and stimulus adaptation properties of monoptic and dichoptic COS. We found that dichoptic COS is best elicited with lower temporal frequencies and is substantially reduced after prolonged adaptation to a mask grating. In contrast, monoptic COS is more pronounced with mask gratings at much higher temporal frequencies and is less prone to stimulus adaptation. These results suggest that monoptic COS is mediated by subcortical mechanisms, whereas intracortical inhibition is the mechanism for dichoptic COS.