Recent reports of the lack of periodic orientation columns in a very large rodent species, the red-rumped agouti, and the existence of incompressible hypercolumns in the lineage of primates, as ...demonstrated in one of the smallest primates, the mouse lemur, strengthen the interpretation that salt-and-pepper and columns-and-pinwheel mosaics are two distinct functional layouts. These layouts do neither depend on lifestyle nor scale with body size, brain size, absolute neuron numbers, binocular overlap, or visual acuity, but are primarily distinguishable by phylogenetic traits. The predictive value of other biological signatures such as V1 neuronal surface density and the central-peripheral density ratio of retinal ganglion cells are reconsidered, and experiments elucidating the intracortical connectivity in rodents are proposed.
•Informed taxon sampling elucidates the dependence of V1 functional architecture on lifestyle, brain size, and lineage.•Orientation-selective neurons appear in one of two categorially distinct layouts, columns-and-pinwheels or salt-and-pepper.•In mammalian V1, salt-and-pepper is the most likely ancestral condition.•In support of a punctuated equilibrium mode for V1 circuits, both layouts exhibit minimal intra-lineage differences.•Circuit level theories associate salt-and-pepper with random and columns-and-pinwheels with orientation-selective wiring.
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.
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.
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.
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.
•We describe four streams of visual information processing in primates.•Retinotopic maps do not translate into visual perception.•The maps of the ventral stream visual areas are visuotopic, and reconstruct the representation of the visual scene by perceptual completion and filling in.•The topography of the visual maps is the basis for a dynamic network responsible for a craniocentric representation.•Visual perception is dynamic, abstract, and not necessarily rooted in a concrete physical reality.
Long-range horizontal connections are thought to modulate the responsiveness of neurons by supplying contextual information. A special type of long-range connections are interhemispheric projections, ...linking the 2 cerebral hemispheres. To investigate the action of those projections in a causal approach, we recorded in cat primary visual cortex while deactivating corresponding regions on the contralateral hemisphere. Interestingly, the action of callosal projections turned out to depend on the local and global composition of the stimulus: Full-field stimulation with gratings revealed moderate rate decreases (modulation index -0.24) and some significant increases (+0.21), whereas with lesser salient random dot textures, much more neurons were affected and reacted with pronounced rate decreases (-0.4). However, orientation and direction selectivity of those neurons were only slightly influenced by callosal input. This invariance could be achieved by scaling responses multiplicatively. Indeed, we could quantify the action of callosal input as a multiplicative scaling of responses, but additive scaling also occurred, especially for grating stimulation. We conclude that the quantitative action of long-range horizontal connections is by no means fixed but depends on how the network is driven by an external stimulus. Qualitatively, those connections seem to adjust the response gain of neurons, thereby preserving their selectivity.
Functional imaging methods monitor neural activity by measuring hemodynamic signals. These are more closely related to local field potentials (LFPs) than to action potentials. We simultaneously ...recorded electrical and hemodynamic responses in the cat visual cortex. Increasing stimulus strength enhanced spiking activity, high-frequency LFP oscillations, and hemodynamic responses. With constant stimulus intensity, the hemodynamic response fluctuated; these fluctuations were only loosely related to action potential frequency but tightly correlated to the power of LFP oscillations in the gamma range. These oscillations increase with the synchrony of synaptic events, which suggests a close correlation between hemodynamic responses and neuronal synchronization.
Neurons in the cerebral cortex are constantly integrating different types of inputs. Dependent on their origin, these inputs can be modulatory in many ways and, for example, change the neuron's ...responsiveness, sensitivity, or selectivity. To investigate the modulatory role of lateral input from the same level of cortical hierarchy, we recorded in the primary visual cortex of cats while controlling synaptic input from the corresponding contralateral hemisphere by reversible deactivation. Most neurons showed a pronounced decrease in their response to a visual stimulus of different contrasts and orientations. This indicates that the lateral network acts via an unspecific gain-setting mechanism, scaling the output of a neuron. However, the interhemispheric input also changed the contrast sensitivity of many neurons, thereby acting on the input. Such a contrast gain mechanism has important implications because it extends the role of the lateral network from pure response amplification to the modulation of a specific feature. Interestingly, for many neurons, we found a mixture of input and output gain modulation. Based on these findings and the known physiology of callosal connections in the visual system, we developed a simple model of lateral interhemispheric interactions. We conclude that the lateral network can act directly on its target, leading to a sensitivity change of a specific feature, while at the same time it also can act indirectly, leading to an unspecific gain setting. The relative contribution of these direct and indirect network effects determines the outcome for a particular neuron.
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.
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.
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