On the Functional Role of Gamma Synchronization in the Retinogeniculate System of the Cat.

Fast gamma oscillations, generated within the retina, and transmitted to the cortex via the lateral geniculate nucleus (LGN), are thought to carry information about stimulus size and continuity. This hypothesis relies mainly on studies conducted under anesthesia and the extent to which it holds under more naturalistic conditions remains unclear. Using multielectrode recordings of spiking activity in the retina and the LGN of both male and female cats, we show that visually driven gamma oscillations are absent for awake states and are highly dependent on halothane (or isoflurane). Under ketamine, responses were nonoscillatory, as in the awake condition. Response entrainment to the monitor refresh was commonly observed up to 120 Hz and was superseded by the gamma oscillatory responses induced by halothane. Given that retinal gamma oscillations are contingent on halothane anesthesia and absent in the awake cat, such oscillations should be considered artifactual, thus playing no functional role in vision.SIGNIFICANCE STATEMENT Gamma rhythms have been proposed to be a robust encoding mechanism critical for visual processing. In the retinogeniculate system of the cat, many studies have shown gamma oscillations associated with responses to static stimuli. Here, we extend these observations to dynamic stimuli. An unexpected finding was that retinal gamma responses strongly depend on halothane concentration levels and are absent in the awake cat. These results weaken the notion that gamma in the retina is relevant for vision. Notably, retinal gamma shares many of the properties of cortical gamma. In this respect, oscillations induced by halothane in the retina may serve as a valuable preparation, although artificial, for studying oscillatory dynamics.

Cortical maps as a fundamental neural substrate for visual representation.

Visual perception is the product of serial hierarchical processing, parallel processing, and remapping on a dynamic network involving several topographically organized cortical visual areas. Here, we will focus on the topographical organization of cortical areas and the different kinds of visual maps found in the primate brain. We will interpret our findings in light of a broader representational framework for perception. Based on neurophysiological data, our results do not support the notion that vision can be explained by a strict representational model, where the objective visual world is faithfully represented in our brain. On the contrary, we find strong evidence that vision is an active and constructive process from the very initial stages taking place in the eye and from the very initial stages of our development. A constructive interplay between perceptual and motor systems (e.g., during saccadic eye movements) is actively learnt from early infancy and ultimately provides our fluid stable visual perception of the world.

Altered brain connectivity during visual stimulation in schizophrenia.

Schizophrenia (SCZ) can be described as a functional dysconnectivity syndrome that affects brain connectivity and circuitry. However, little is known about how sensory stimulation modulates network parameters in schizophrenia, such as their small-worldness (SW) during visual processing. To address this question, we applied graph theory algorithms to multi-electrode EEG recordings obtained during visual stimulation with a checkerboard pattern-reversal stimulus. Twenty-six volunteers participated in the study, 13 diagnosed with schizophrenia (SCZ; mean age = 38.3 years; SD = 9.61 years) and 13 healthy controls (HC; mean age = 28.92 years; SD = 12.92 years). The visually evoked potential (VEP) showed a global amplitude decrease (p < 0.05) for SCZ patients as opposed to HC but no differences in latency (p > 0.05). As a signature of functional connectivity, graph measures were obtained from the Magnitude-Squared Coherence between signals from pairs of occipital electrodes, separately for the alpha (8-13 Hz) and low-gamma (36-55 Hz) bands. For the alpha band, there was a significant effect of the visual stimulus on all measures (p < 0.05) but no group interaction between SCZ and HZ (p > 0.05). For the low-gamma spectrum, both groups showed a decrease of Characteristic Path Length (L) during visual stimulation (p < 0.05), but, contrary to the HC group, only SCZ significantly lowered their small-world (SW) connectivity index during visual stimulation (SCZ p < 0.05; HC p > 0.05). This indicates dysconnectivity of the functional network in the low-gamma band of SCZ during stimulation, which might indirectly reflect an altered ability to react to new sensory input in patients. These results provide novel evidence about a possible electrophysiological signature of the global deficits revealed by the application of graph theory onto electroencephalography in schizophrenia.

Spatial clustering of orientation preference in primary visual cortex of the large rodent agouti.

All rodents investigated so far possess orientation-selective neurons in the primary visual cortex (V1) but - in contrast to carnivores and primates - no evidence of periodic maps with pinwheel-like structures. Theoretical studies debating whether phylogeny or universal principles determine development of pinwheels point to V1 size as a critical constraint. Thus, we set out to study maps of agouti, a big diurnal rodent with a V1 size comparable to cats'. In electrophysiology, we detected interspersed orientation and direction-selective neurons with a bias for horizontal contours, corroborated by homogeneous activation in optical imaging. Compatible with spatial clustering at short distance, nearby neurons tended to exhibit similar orientation preference. Our results argue against V1 size as a key parameter in determining the presence of periodic orientation maps. They are consistent with a phylogenetic influence on the map layout and development, potentially reflecting distinct retinal traits or interspecies differences in cortical circuitry.

Callosal Influence on Visual Receptive Fields Has an Ocular, an Orientation-and Direction Bias.

One leading hypothesis on the nature of visual callosal connections (CC) is that they replicate features of intrahemispheric lateral connections. However, CC act also in the central part of the binocular visual field. In agreement, early experiments in cats indicated that they provide the ipsilateral eye part of binocular receptive fields (RFs) at the vertical midline (Berlucchi and Rizzolatti, 1968), and play a key role in stereoscopic function. But until today callosal inputs to receptive fields activated by one or both eyes were never compared simultaneously, because callosal function has been often studied by cutting or lesioning either corpus callosum or optic chiasm not allowing such a comparison. To investigate the functional contribution of CC in the intact cat visual system we recorded both monocular and binocular neuronal spiking responses and receptive fields in the 17/18 transition zone during reversible deactivation of the contralateral hemisphere. Unexpectedly from many of the previous reports, we observe no change in ocular dominance during CC deactivation. Throughout the transition zone, a majority of RFs shrink, but several also increase in size. RFs are significantly more affected for ipsi- as opposed to contralateral stimulation, but changes are also observed with binocular stimulation. Noteworthy, RF shrinkages are tiny and not correlated to the profound decreases of monocular and binocular firing rates. They depend more on orientation and direction preference than on eccentricity or ocular dominance of the receiving neuron's RF. Our findings confirm that in binocularly viewing mammals, binocular RFs near the midline are constructed via the direct geniculo-cortical pathway. They also support the idea that input from the two eyes complement each other through CC: Rather than linking parts of RFs separated by the vertical meridian, CC convey a modulatory influence, reflecting the feature selectivity of lateral circuits, with a strong cardinal bias.

Motion contrast in primary visual cortex: a direct comparison of single neuron and population encoding.

Features from outside the classical receptive field (CRF) can modulate the stimulus-driven activity of single cells in the primary visual cortex. This modulation, mediated by horizontal and feedback networks, has been extensively described as a variation of firing rate and is considered the basis of processing features as, for example, motion contrast. However, surround influences have also been identified in pairwise spiking or local field coherence. Yet, evidence about co-existence and integration of different neural signatures remains elusive. To compare multiple signatures, we recorded spiking and LFP activity evoked by stimuli exhibiting a motion contrast in the CRFs surround in anesthetized cat primary visual cortex. We chose natural-like scenes over gratings to avoid predominance of simple visual features, which could be easily represented by a rate code. We analyzed firing rates and phase-locking to low-gamma frequency in single cells and neuronal assemblies. Motion contrast was reflected in all measures but in semi-independent populations. Whereas activation of assemblies accompanied single neuron rates, their phase relations were modulated differently. Interestingly, only assembly phase relations mirrored the direction of movement of the surround and were selectively affected by thermal deactivation of visual interhemispheric connections. We argue that motion contrast can be reflected in complementary and superimposed neuronal signatures that can represent different surround features in independent neuronal populations.

Selective interhemispheric circuits account for a cardinal bias in spontaneous activity within early visual areas.

Ongoing brain activity exhibits patterns resembling neural ensembles co-activated by stimulation or task performance. Such patterns have been attributed to the brain's functional architecture, e.g. selective long-range connections. Here, we directly investigate the contribution of selective connections between hemispheres to spontaneous and evoked maps in cat area 18 close to the 17/18 border. We recorded voltage-sensitive dye imaging maps and spiking activity while manipulating interhemispheric input by reversibly deactivating corresponding contralateral areas. During deactivation, spontaneous maps continued to be generated with similar frequency and quality as in the intact network but a baseline cardinal bias disappeared. Consistently, neurons preferring either horizontal (HN) or vertical (VN), as opposed to oblique contours, decreased their resting state activity. HN decreased their rates also when stimulated visually. We conclude that structured spontaneous maps are primarily generated by thalamo- and/or intracortical connectivity. However, selective long-range connections through the corpus callosum - in perpetuation of the long-range intracortical network - contribute to a cardinal bias, possibly, because they are stronger or more frequent between neurons preferring horizontal and/or cardinal contours. As those contours are easier perceived and appear more frequently in natural environment, long-range connections might provide visual cortex with a grid for probabilistic grouping operations in a larger visual scene.

An updated midline rule: visual callosal connections anticipate shape and motion in ongoing activity across the hemispheres.

It is generally thought that callosal connections (CCs) in primary visual cortices serve to unify the visual scenery parted in two at the vertical midline (VM). Here, we present evidence that this applies also to visual features that do not cross yet but might cross the VM in the future. During reversible deactivation of the contralateral visual cortex in cats, we observed that ipsilaterally recorded neurons close to the border between areas 17 and 18 receive selective excitatory callosal input on both ongoing and evoked activity. In detail, neurons responding well to a vertical Gabor patch moving away from the deactivated hemifield decreased prestimulus and stimulus-driven activity much more than those preferring motion toward the cooled hemifield. Further, activity of neurons responding to horizontal lines decreased more than the response to vertical lines. Embedding a single Gabor into a collinear line context selectively stabilized responses, especially when the context was limited to the intact hemifield. These findings indicate that CCs interconnect not only neurons coding for similar orientations but also for similar directions of motion. We conclude that CCs anticipate stimulus features that are potentially relevant for both hemifields (i.e., coherent motion but also collinear shape) because already prestimulus activity and activity to stimuli not crossing the VM revealed feature specificity. Finally, we hypothesize that intrinsic and callosal networks processing different orientations and directions are anisotropic close to the VM facilitating perceptual grouping along likely future motion or (shape) trajectories before the visual stimulus arrives.

The visual callosal connection: a connection like any other?

Recent work about the role of visual callosal connections in ferrets and cats is reviewed, and morphological and functional homologies between the lateral intrinsic and callosal network in early visual areas are discussed. Both networks selectively link distributed neuronal groups with similar response properties, and the actions exerted by callosal input reflect the functional topography of those networks. This supports the notion that callosal connections perpetuate the function of the lateral intrahemispheric circuit onto the other hemisphere. Reversible deactivation studies indicate that the main action of visual callosal input is a multiplicative shift of responses rather than a changing response selectivity. Both the gain of that action and its excitatory-inhibitory balance seem to be dynamically adapted to the feedforward drive by the visual stimulus onto primary visual cortex. Taken together anatomical and functional evidence from corticocortical and lateral circuits further leads to the conclusion that visual callosal connections share more features with lateral intrahemispheric connections on the same hierarchical level and less with feedback connections. I propose that experimental results about the callosal circuit in early visual areas can be interpreted with respect to lateral connectivity in general.