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Previous work has established that the spatial receptive fields (SRFs) of multisensory neurons in the cerebral cortex are strikingly heterogeneous, and that SRF architecture plays an important deterministic role in sensory responsiveness and multisensory integrative capacities. The initial part of this contribution serves to review these findings detailing the key features of SRF organization in cortical multisensory populations by highlighting work from the cat anterior ectosylvian sulcus (AES). In addition, we have recently conducted parallel studies designed to examine SRF architecture in the classic model for multisensory studies, the cat superior colliculus (SC), and we present some of the preliminary observations from the SC here. An examination of individual SC neurons revealed marked similarities between their unisensory (i.e., visual and auditory) SRFs, as well as between these unisensory SRFs and the multisensory SRF. Despite these similarities within individual neurons, different SC neurons had SRFs that ranged from a single area of greatest activation (hot spot) to multiple and spatially discrete hot spots. Similar to cortical multisensory neurons, the interactive profile of SC neurons was correlated strongly to SRF architecture, closely following the principle of inverse effectiveness. Thus, large and often superadditive multisensory response enhancements were typically seen at SRF locations where visual and auditory stimuli were weakly effective. Conversely, subadditive interactions were seen at SRF locations where stimuli were highly effective. Despite the unique functions characteristic of cortical and subcortical multisensory circuits, our results suggest a strong mechanistic interrelationship between SRF microarchitecture and integrative capacity.

Several studies have shown that neurons with similar response properties are arranged together in domains across primary visual cortex (V1). An orderly pattern of domains has been described for preferences to ocular dominance, orientation, and spatial frequency. Temporal frequency preference, another important attribute of the visual scene, also might be expected to map into different domains. Using optical imaging and a variety of quantitative methods, we examined how temporal frequency selectivity is mapped in V1 of the prosimian primate, bush baby (Otolemur garnetti). We found that unlike other attribute maps, selectivity for different temporal frequencies is arranged uniformly across V1 with no evidence of local clustering. Global tuning for temporal frequency, based on magnitude of response, showed a good match to previous tuning curves for single neurons. A peak response was found around 2.0 Hz, with smaller attenuation at lower temporal frequencies than at higher frequencies. We also examined whether the peak temporal frequency response differed between anatomical compartments defined by cytochrome oxidase (CO). No significant differences in the preference for temporal frequency were found between these CO compartments. Our findings show that key sensory attributes that are linked in perception can be organized in quite distinct ways in V1 of primates.

It has been proposed that low-threshold Ca2+ (LT)-associated bursts in the lateral geniculate nucleus (LGN) of awake animals communicate significant or unexpected visual events to cortex. The present study investigated this hypothesis by examining the incidence of LT bursts in 146 cells recorded from the LGN of three macaque monkeys. Bursts were defined as clusters of two or more action potentials separated by not more than 4 ms and preceded by a ≥100-ms quiescent interval. The incidence of bursts was examined in several intensive-training Go-NoGo and target selection tasks as well as in training-free tasks where natural scenes with both familiar and novel contents were shown. Our chief findings were as follows. 1) Bursts occur in the majority of cells under every condition tested, 2) burst incidence is very low (

Purpose: Previous work has established that the integrative capacity of multisensory neurons in the superior colliculus (SC) matures over a protracted period of postnatal life (Wallace and Stein, 1997), and that the development of normal patterns of multisensory integration depends critically on early sensory experience (Wallace et al., 2004). Although these studies demonstrated the importance of early sensory experience in the creation of mature multisensory circuits, it remains unknown whether the reestablishment of sensory experience in adulthood can reverse these effects and restore integrative capacity. Methods: The current study tested this hypothesis in cats that were reared in absolute darkness until adulthood and then returned to a normal housing environment for an equivalent period of time. Single unit extracellular recordings targeted multisensory neurons in the deep layers of the SC, and analyses were focused on both conventional measures of multisensory integration and on more recently developed methods designed to characterize spatiotemporal receptive fields (STRF). Results: Analysis of the STRF structure and integrative capacity of multisensory SC neurons revealed significant modifications in the temporal response dynamics of multisensory responses (e.g., discharge durations, peak firing rates, and mean firing rates), as well as significant changes in rates of spontaneous activation and degrees of multisensory integration. Conclusions: These results emphasize the importance of early sensory experience in the establishment of normal multisensory processing architecture and highlight the limited plastic potential of adult multisensory circuits.

The functional architecture of sensory brain regions reflects an ingenious biological solution to the competing demands of a continually changing sensory environment. While they are malleable, they have the constancy necessary to support a stable sensory percept. How does the functional organization of sensory brain regions contend with these antithetical demands? Here we describe the functional organization of auditory and multisensory (i.e., auditory-visual) information processing in three sensory brain structures: (1) a low-level unisensory cortical region, the primary auditory cortex (A1); (2) a higher-order multisensory cortical region, the anterior ectosylvian sulcus (AES); and (3) a multisensory subcortical structure, the superior colliculus (SC). We then present a body of work that characterizes the ontogenic expression of experience-dependent influences on the operations performed by the functional circuits contained within these regions. We will present data to support the hypothesis that the competing demands for plasticity and stability are addressed through a developmental transition in operational properties of functional circuits from an initially labile mode in the early stages of postnatal development to a more stable mode in the mature brain that retains the capacity for plasticity under specific experiential conditions. Finally, we discuss parallels between the central tenets of functional organization and plasticity of sensory brain structures drawn from animal studies and a growing literature on human brain plasticity and the potential applicability of these principles to the audiology clinic.

Recent electrophysiology studies have suggested that neuronal responses to multisensory stimuli may possess a unique temporal signature. To evaluate this temporal dynamism, unisensory and multisensory spatiotemporal receptive fields (STRFs) of neurons in the cortex of the cat anterior ectosylvian sulcus were constructed. Analyses revealed that the multisensory STRFs of these neurons differed significantly from the component unisensory STRFs and their linear summation. Most notably, multisensory responses were found to have higher peak firing rates, shorter response latencies, and longer discharge durations. More importantly, multisensory STRFs were characterized by two distinct temporal phases of enhanced integration that reflected the shorter response latencies and longer discharge durations. These findings further our understanding of the temporal architecture of cortical multisensory processing, and thus provide important insights into the possible functional role(s) played by multisensory cortex in spatially directed perceptual processes.

Investigations of multisensory processing at the level of the single neuron have illustrated the importance of the spatial and temporal relationship of the paired stimuli and their relative effectiveness in determining the product of the resultant interaction. Although these principles provide a good first-order description of the interactive process, they were derived by treating space, time, and effectiveness as independent factors. In the anterior ectosylvian sulcus (AES) of the cat, previous work hinted that the spatial receptive field (SRF) architecture of multisensory neurons might play an important role in multisensory processing due to differences in the vigor of responses to identical stimuli placed at different locations within the SRF. In this study the impact of SRF architecture on cortical multisensory processing was investigated using semichronic single-unit electrophysiological experiments targeting a multisensory domain of the cat AES. The visual and auditory SRFs of AES multisensory neurons exhibited striking response heterogeneity, with SRF architecture appearing to play a major role in the multisensory interactions. The deterministic role of SRF architecture was tightly coupled to the manner in which stimulus location modulated the responsiveness of the neuron. Thus multisensory stimulus combinations at weakly effective locations within the SRF resulted in large (often superadditive) response enhancements, whereas combinations at more effective spatial locations resulted in smaller (additive/subadditive) interactions. These results provide important insights into the spatial organization and processing capabilities of cortical multisensory neurons, features that may provide important clues as to the functional roles played by this area in spatially directed perceptual processes.

It has recently been demonstrated that the maturation of normal multisensory circuits in the cortex of the cat takes place over an extended period of postnatal life. Such a finding suggests that the sensory experiences received during this time may play an important role in this developmental process. To test the necessity of sensory experience for normal cortical multisensory development, cats were raised in the absence of visual experience from birth until adulthood, effectively precluding all visual and visual–nonvisual multisensory experiences. As adults, semichronic single-unit recording experiments targeting the anterior ectosylvian sulcus (AES), a well-defined multisensory cortical area in the cat, were initiated and continued at weekly intervals in anesthetized animals. Despite having very little impact on the overall sensory representations in AES, dark-rearing had a substantial impact on the integrative capabilities of multisensory AES neurons. A significant increase was seen in the proportion of multisensory neurons that were modulated by, rather than driven by, a second sensory modality. More important, perhaps, there was a dramatic shift in the percentage of these modulated neurons in which the pairing of weakly effective and spatially and temporally coincident stimuli resulted in response depressions. In normally reared animals such combinations typically give rise to robust response enhancements. These results illustrate the important role sensory experience plays in shaping the development of mature multisensory cortical circuits and suggest that dark-rearing shifts the relative balance of excitation and inhibition in these circuits.

There is significant controversy regarding the ability of the primate visual system to construct stable percepts from a never-ending stream of brief fixations and rapid saccadic eye movements. In this study, we examined the timing and occurrence of perisaccadic modulation of LGN single-unit activity in awake-behaving macaque monkeys while they made spontaneous saccades in the dark and made visually guided saccades to discrete stimuli located outside the receptive field. Our hypothesis was that the activity of LGN cells is modulated by efference copies of motor plans to produce saccadic eye movements and that this modulation depends neither on the presence of feedforward visual information nor on a corollary discharge of signals directing saccadic eye movements. On average, 25% of LGN cells demonstrated significant perisaccadic modulation. This modulation consisted of a moderate suppression of activity that began more than 100 ms prior to the initiation of a saccadic eye movement and continued beyond the termination of the saccadic eye movement. This suppression was followed by a large enhancement of activity after the eyes arrived at the next fixation. Although members of all three LGN relay cell classes (magnocellular, parvocellular, and koniocellular) demonstrated significant saccade-related suppression and enhancement of activity, more cells demonstrated postsaccadic enhancement (25%) than perisaccadic suppression (17%). In no case did the timing of the modulation coincide directly with saccade duration. The degree of modulation observed did not vary with LGN cell class, LGN receptive field center location, center sign (ON-center or OFF-center), or saccade latency or velocity. The time course of modulation did, however, vary with saccade size such that suppression was longer for longer saccades. The fact that activity from a percentage of LGN cells from all cell classes was modulated in relationship to saccadic eye movements in the absence of direct visual stimulation suggests that this modulation is a general phenomenon not tied to specific types of visual stimuli. Similarly, because the onset of the modulation preceded eye movements by more than 100 ms, it is likely that this modulation reflects higher order motor-planning rather than a corollary of mechanisms in direct control of eye movements themselves. Finally, the fact that the largest modulation is a postsaccadic enhancement of activity may suggest that perisaccadic modulations are designed more for the facilitation of visual information processing once the eyes land at a new location than for filtering unwanted visual stimuli.