Search

The visual cortex of carnivores and primates displays a high degree of modular network organization characterized by local clustering and structured long-range correlations of activity and functional properties. Excitatory networks display modular organization before the onset of sensory experience, but the developmental timeline for modular networks of GABAergic interneurons remains under-explored. Using in vivo calcium imaging of the ferret visual cortex, we find evidence that before visual experience, interneurons display weak orientation tuning and widespread, correlated activity in response to visual stimuli. Robust modular organization and orientation tuning are evident with as little as one week of visual experience. Furthermore, we find that the maturation of orientation tuning requires visual experience, while the reduction in widespread, correlated network activity does not. Thus, the maturation of inhibitory cortical networks occurs in a delayed, parallel process relative to excitatory neurons. Excitatory neurons in the carnivore and primate visual cortex display orientation selectivity arranged in a modular fashion before the onset of visual experience, but the developmental timeline for visual response selectivity of inhibitory neurons is unknown. Using in vivo calcium imaging in ferret visual cortex, the authors show that experience-dependent emergence of orientation selectivity develops in a modular fashion for inhibitory interneurons over the first week of visual experience. [ABSTRACT FROM AUTHOR]

Visual experience plays a critical role in the development of direction-selective responses in ferret visual cortex. In visually naive animals, presentation of a bidirectional "training" stimulus induces rapid increases in the direction-selective responses of single neurons that can be predicted by small but significant direction biases that are present in neighboring neurons at the onset of stimulation. In this study we used in vivo two-photon imaging of calcium signals to further explore the contribution of visual experience to the emergence of directionselective responses in ferret visual cortex. The first set of experiments was designed to determine whether visual experience is required for the development of the initial neighborhood bias. In animals that were dark-reared until the time of eye opening, we found that individual neurons exhibited weak direction-selective responses accompanied by a reduced but statistically significant neighborhood bias, indicating that both features arise without the need for visual experience. The second set of experiments used a unidirectional training stimulus to assess the relative roles of the neighborhood bias and visual experience in determining the direction preference that cortical neurons acquire during direction training. We found that neurons became more responsive to the trained direction even when they were located in regions of the cortex with an initial neighborhood bias for the direction opposite the training stimulus. Together, these results suggest an adaptive developmental strategy for the elaboration of direction-selective responses, one in which experience-independent mechanisms provide a symmetry-breaking seed for the instructive effects of visual experience. [ABSTRACT FROM AUTHOR]

Stimulus features such as edge orientation, motion direction and spatial frequency are thought to be encoded in the primary visual cortex by overlapping feature maps arranged so that the location of neurons activated by a particular combination of stimulus features can be predicted from the intersections of these maps. This view is based on the use of grating stimuli, which limit the range of stimulus combinations that can be examined. We used optical imaging of intrinsic signals in ferrets to assess patterns of population activity evoked by the motion of a texture (a field of iso-oriented bars). Here we show that the same neural population can be activated by multiple combinations of orientation, length, motion axis and speed. Rather than reflecting the intersection of multiple maps, our results indicate that population activity in primary visual cortex is better described as a single map of spatiotemporal energy. [ABSTRACT FROM AUTHOR]

In visual cortex, signals from the two eyes merge to form a coherent binocular representation. Here we investigate the synaptic interactions underlying the binocular representation of stimulus orientation in ferret visual cortex with in vivo calcium imaging of layer 2/3 neurons and their dendritic spines. Individual neurons with aligned somatic responses received a mixture of monocular and binocular synaptic inputs. Surprisingly, monocular pathways alone could not account for somatic alignment because ipsilateral monocular inputs poorly matched somatic preference. Binocular inputs exhibited different degrees of interocular alignment, and those with a high degree of alignment (congruent) had greater selectivity and somatic specificity. While congruent inputs were similar to others in measures of strength, simulations show that the number of active congruent inputs predicts aligned somatic output. Our study suggests that coherent binocular responses derive from connectivity biases that support functional amplification of aligned signals within a heterogeneous binocular intracortical network. [Display omitted] • Layer 2/3 neurons in visual cortex receive monocular and binocular synaptic inputs • Monocular inputs alone cannot account for somatic binocular alignment • Binocular congruent inputs exhibit functional properties ideally suited for alignment • Dominant influence of binocular congruent inputs derives from strength in numbers Scholl, Tepohl, et al. investigate how signals from the two eyes are combined within synaptic populations of individual neurons to shape a coherent representation. Rather than a convergence of monocular streams, they find that intracortical binocular networks are key to shaping alignment in cortical layer 2/3. [ABSTRACT FROM AUTHOR]

Understanding how cortical inhibition shapes circuit function requires identifying the connectivity rules relating the response properties of inhibitory interneurons and their postsynaptic targets. Here we explore the orientation tuning of layer 2/3 inhibitory inputs in the ferret visual cortex using a combination of in vivo axon imaging, functional input mapping, and physiology. Inhibitory boutons exhibit robust orientation-tuned responses with preferences that can differ significantly from the cortical column in which they reside. Inhibitory input fields measured with patterned optogenetic stimulation and intracellular recordings revealed that these inputs originate from a wide range of orientation domains, inconsistent with a model of co-tuned inhibition and excitation. Intracellular synaptic conductance measurements confirm that individual neurons can depart from a co-tuned regime. Our results argue against a simple rule for the arrangement of inhibitory inputs supplied by layer 2/3 circuits and suggest that heterogeneity in presynaptic inhibitory networks contributes to neural response properties. • GABAergic boutons have diverse orientation preferences within orientation domains • Single-neuron inhibitory input fields originate from diverse orientation domains • Conductance measurements show inhibition and excitation are not strictly co-tuned Scholl et al. examine the functional connectivity of layer 2/3 inhibitory inputs onto single neurons in the ferret visual cortex. This study argues against a simple rule describing the arrangement of inhibitory inputs supplied by layer 2/3 circuits. [ABSTRACT FROM AUTHOR]

Summary Functional circuits in the visual cortex require the coordinated activity of excitatory and inhibitory neurons. Molecular genetic approaches in the mouse have led to the “local non-specific pooling principle” of inhibitory connectivity, in which inhibitory neurons are untuned for stimulus features due to the random pooling of local inputs. However, it remains unclear whether this principle generalizes to species with a columnar organization of feature selectivity such as carnivores, primates, and humans. Here we use virally mediated GABAergic-specific GCaMP6f expression to demonstrate that inhibitory neurons in ferret visual cortex respond robustly and selectively to oriented stimuli. We find that the tuning of inhibitory neurons is inconsistent with the local non-specific pooling of excitatory inputs and that inhibitory neurons exhibit orientation-specific noise correlations with local and distant excitatory neurons. These findings challenge the generality of the non-specific pooling principle for inhibitory neurons, suggesting different rules for functional excitatory-inhibitory interactions in non-murine species. [ABSTRACT FROM AUTHOR]