Contrast‐dependent OFF‐dominance in cat primary visual cortex facilitates discrimination of stimuli with natural contrast statistics

Both theoretical and experimental studies suggest that response properties in the visual system are shaped by signals in the natural environment. Recent studies showed that, in the primary visual cortex (V1), neurons preferring light decrements (OFF stimuli) outnumber those preferring light increments (ON stimuli). However, it is not clear whether the OFF‐dominance in V1 neurons is related to the contrast statistics in natural images. By analysing the distribution of negative and positive contrasts in natural images at several spatial scales, we showed that optimal coding of the natural contrast signals would lead to a contrast‐dependent OFF‐dominant response, with a stronger degree of OFF‐dominance at a higher contrast. Using bright and dark stimuli at various contrast levels to measure the receptive fields of neurons in cat V1, we found an increasing degree of OFF‐dominance of the neuronal population as the contrast was increased. By modeling receptive fields exhibiting OFF‐ and ON‐dominance, we found that contrast‐dependent OFF‐dominance facilitated the discrimination of stimuli with natural contrast distribution. Thus, by matching contrast‐dependent OFF‐dominance to the statistics of contrast distribution in natural images, V1 neurons may better discriminate contrast information in natural scenes.     

Comparison of the selectivity of postsynaptic potentials and spike responses in cat visual cortex

Intracellular recordings were made from neurons in the cat visual cortex (area 17) to compare the orientation and direction selectivities of the output of a cell with those of the input the cell receives. The input to a cell was estimated from the PSPs (postsynaptic potentials) evoked by visual stimulation, and the output estimated from the number of spikes generated during the same responses. For the whole sample, selectivity of the output of cells was significantly higher than selectivity of their input. Upon PSP to spike transformation, the selectivity index was, on average, doubled. However, the degree of the selectivity improvement in individual cells was very different, varying from cases in which highly selective output was created from a poorly selective input and thus selectivity was greatly improved, to little or no improvement in other neurons. The improvement of selectivity was not correlated with resting membrane potential, threshold for action potential generation, background discharge rate or amplitude of optimal PSP response. Further, no systematic difference was found between simple and complex cells in the input-output relations, indicating that the 'tip of the iceberg' effect on shaping the response selectivity was cell specific, but not cell type specific. This supports the notion that multiple mechanisms are responsible for generation of the response selectivity, and that the contribution of any particular mechanism may vary from one cell to the other. The heterogeneity of the input-output relations in visual cortical cells could indicate different functions of cells in the cortical network; some cells are creating selectivity de novo, the function of other neurons probably being repetition and amplification of the selected signal and arrangement of the output of a whole column.     

Spike synchronization in cat primary visual cortex depends on similarity of surround‐suppression magnitude

In the primary visual cortex (V1), the spike synchronization seen in neuron pairs with non‐overlapping receptive fields can be explained by similarities in their preferred orientation (PO). However, this is not true for pairs with overlapping receptive fields, as they can still exhibit spike synchronization even if their POs are only weakly correlated. Here, we investigated the relationship between spike synchronization and suppressive modulation derived from classical receptive‐field surround (surround suppression). We found that layer 4 and layer 2/3 pairs exhibited mainly asymmetric spike synchronization that had non‐zero time‐lags and was dependent on both the similarity of the PO and the strength of surround suppression. In contrast, layer 2/3 and layer 2/3 pairs showed mainly symmetric spike synchronization that had zero time‐lag and was dependent on the similarity of the strength of surround suppression but not on the similarity in POs. From these results, we propose that in cat V1 there exists a functional network that mainly depends on the similarity in surround suppression, and that in layer 2/3 neurons the network maintains surround suppression that is primarily inherited from layer 4 neurons.     

Regional variation in the representation of the visual field in the visual cortex of the siamese cat

In Siamese cats, many ganglion cell fibers from the temporal retina misproject to the contralateral hemisphere; as a result, each lateral geniculate nucleus contains an abnormally large representation of the ipsilateral visual field. The manner in which the visual cortex processes this aberrant visual information has been examined in several previous studies. In some Siamese cats, the region of the 17/18 border was found to contain an extensive, systematic map of the ipsilateral field, while in other animals no such map was found, and the 17/18 border appeared to represent the zero meridian of azimuth (as in normal cats). These results have led to the suggestion that there are two distinct types of Siamese cat (“Boston” and “Midwestern”) which can be distinguished on the basis of cortical topography and the anatomical organization of the geniculocortical pathway. In the present study, we have recorded from four Siamese cats in order to examine the visual field map in the region of the 17/18 border; in each cat we recorded at anterior coronal levels corresponding to the representation of the lower visual field, and also at more posterior levels near the horizontal meridian representation. In all of the animals we found that the anterior penetrations (corresponding to mean receptive field elevations inferior to ?7°) yielded 15–20° of ipsilateral field representation at the 17/18 border; however, the posterior, horizontal meridian penetrations (with mean elevations from +1° to ?4°) showed excursions of only about 5° into the ipsilateral field. This large difference in the representation of azimuth was not due to rotation of the eyes during our recording sessions. The finding of appreciable differences in the amount of ipsilateral field represented at different anterior-posterior levels of the same animal might lead to the suggestion that there are not two distinct populations (or types) of Siamese cat with regard to the cortical map of the ipsilateral field. Rather, we raise the possibility that Siamese cats form one population in which there is a continuous variation in the extent of ipsilateral field represented in the cortex.     

Direction selectivity of neurons in the visual cortex is non‐linear and lamina‐dependent

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.     

Fluoxetine and serotonin facilitate attractive‐adaptation‐induced orientation plasticity in adult cat visual cortex

Neurons in V1 display orientation selectivity by responding optimally to a preferred orientation edge when it is presented within their receptive fields. Orientation plasticity in striate cortex occurs either by ocular deprivation or by imposition of a non‐preferred stimulus for several minutes. Adaptation of neurons to a non‐optimal orientation induces shifts of tuning curves towards the adapting orientation (attractive shift) or away from it (repulsive shift). Here, we investigated the effects of the neurotransmitter serotonin and antidepressant fluoxetine (a selective serotonin reuptake inhibitor) on the modulation of adaptation‐induced orientation plasticity. We show that serotonin and fluoxetine promote mostly attractive shifts. Attractive shifts augmented in magnitude towards adapter, whereas repulsive neurons reversed their behavior in the direction of the forced orientation. Furthermore, neurons which retained their original preferred orientation expressed plasticity by shifting their tuning curves after drug administration mostly towards adapter. Our data suggest a pre‐eminent role of fluoxetine by inducing and facilitating short‐term plasticity in V1.     

Stronger responses to darks along the ventral pathway of the cat visual cortex

Light increments (brights) and decrements (darks) are differently processed throughout the early visual system. It is well known that a bias towards faster and stronger responses to darks is present in the retina, lateral geniculate nucleus and primary visual cortex. In humans, psychophysical and neurophysiological data indicate that darks are better detected than brights, suggesting that the dark bias found in early visual areas is transmitted across the cortical hierarchy. Here, we tested this assumption by investigating the spatiotemporal features of responses to brights and darks in area 21a, a gateway area of the cat ventral stream, using reverse correlation analysis of a sparse noise stimulus. The receptive field of most 21a neurons exhibited larger dark subfields. Additionally, the amplitude of the responses to darks was considerably greater than those evoked by brights. In the temporal domain, no differences were found between the response peak latency. Thus, the present study supports the notion that bright/dark asymmetries are transmitted throughout the cortical hierarchy and further, that the luminance processing varies as a function of the position in the cortical hierarchy, dark preference being strongly enhanced (in the spatial domain and response amplitude) along the ventral pathway.     

Diversity of thalamorecipient spine morphology in cat visual cortex and its implication for synaptic plasticity

A feature of spine synapses is the existence of a neck connecting the synapse on the spine head to the dendritic shaft. As with a cable, spine neck resistance (R_neck) increases with increasing neck length and is inversely proportional to the cross‐sectional area of the neck. A synaptic current entering a spine with a high R_neck will lead to greater local depolarization in the spine head than would a similar input applied to a spine with a lower R_neck. This could make spines with high R_neck more sensitive to plastic changes since voltage sensitive conductances, such as N‐methyl‐D‐aspartic acid (NMDA) channels can be more easily activated. This hypothesis was tested using serial section electron microscopic reconstructions of thalamocortical spine synapses and spine necks located on spiny stellate cells and corticothalamic cells from area 17 of cats. Thalamic axons and corticothalamic neurons were labeled by injections of the tracer biotinylated dextran amine (BDA) in the dorsal lateral geniculate nucleus (dLGN) of anesthetized cats and spiny stellates were filled intracellularly in vivo with horseradish peroxidase. Twenty‐eight labeled spines that formed synapses with dLGN boutons were collected from three spiny stellate and four corticothalamic cells and reconstructed in 3D from serial electron micrographs. Spine length, spine diameter, and the area of the postsynaptic density were measured from the 3D reconstructions and R_neck of the spine was estimated. No correlation was found between the postsynaptic density size and the estimated spine R_neck. This suggests that forms of plasticity that lead to larger synapses are independent of spine neck resistance. J. Comp. Neurol. 521:2058–2066, 2013. © 2012 Wiley Periodicals, Inc.     

Context‐dependent coding and gain control in the auditory system of crickets

Sensory systems process stimuli that greatly vary in intensity and complexity. To maintain efficient information transmission, neural systems need to adjust their properties to these different sensory contexts, yielding adaptive or stimulus‐dependent codes. Here, we demonstrated adaptive spectrotemporal tuning in a small neural network, i.e. the peripheral auditory system of the cricket. We found that tuning of cricket auditory neurons was sharper for complex multi‐band than for simple single‐band stimuli. Information theoretical considerations revealed that this sharpening improved information transmission by separating the neural representations of individual stimulus components. A network model inspired by the structure of the cricket auditory system suggested two putative mechanisms underlying this adaptive tuning: a saturating peripheral nonlinearity could change the spectral tuning, whereas broad feed‐forward inhibition was able to reproduce the observed adaptive sharpening of temporal tuning. Our study revealed a surprisingly dynamic code usually found in more complex nervous systems and suggested that stimulus‐dependent codes could be implemented using common neural computations.     

Non‐stimulated regions in early visual cortex encode the contents of conscious visual perception

Predictions shape our perception. The theory of predictive processing poses that our brains make sense of incoming sensory input by generating predictions, which are sent back from higher to lower levels of the processing hierarchy. These predictions are based on our internal model of the world and enable inferences about the hidden causes of the sensory input data. It has been proposed that conscious perception corresponds to the currently most probable internal model of the world. Accordingly, predictions influencing conscious perception should be fed back from higher to lower levels of the processing hierarchy. Here, we used functional magnetic resonance imaging and multivoxel pattern analysis to show that non‐stimulated regions of early visual areas contain information about the conscious perception of an ambiguous visual stimulus. These results indicate that early sensory cortices in the human brain receive predictive feedback signals that reflect the current contents of conscious perception.     

Untethered firing fields and intermittent silences: Why grid‐cell discharge is so variable

Grid cells in medial entorhinal cortex are notoriously variable in their responses, despite the striking hexagonal arrangement of their spatial firing fields. Indeed, when the animal moves through a firing field, grid cells often fire much more vigorously than predicted or do not fire at all. The source of this trial‐to‐trial variability is not completely understood. By analyzing grid‐cell spike trains from mice running in open arenas and on linear tracks, we characterize the phenomenon of “missed” firing fields using the statistical theory of zero inflation. We find that one major cause of grid‐cell variability lies in the spatial representation itself: firing fields are not as strongly anchored to spatial location as the averaged grid suggests. In addition, grid fields from different cells drift together from trial to trial, regardless of whether the environment is real or virtual, or whether the animal moves in light or darkness. Spatial realignment across trials sharpens the grid representation, yielding firing fields that are more pronounced and significantly narrower. These findings indicate that ensembles of grid cells encode relative position more reliably than absolute position.     

A study of tachykinin-immunoreactivity in the cat visual cortex

The localization of tachykinin-immunoreactivity in the cat visual cortex (area 17) was investigated using immunohistochemical methods. Strong laminar specificity was observed, with immunoreactivity highest in layer V, followed by layers I, VI, II and III, and the lowest density in layer IV. Most of the immunoreactive product was localized in neuronal processes. A few immunopositive cell bodies were also present. The immunopositive neurons were non-pyramidal, multipolar, or bipolar in shape, and mostly found in layer V. There were particularly dense immunopositive fibers and varicosities around somata in layer V. These may represent tachykinin-containing presynaptic terminals (boutons). The results provide anatomical evidence that tachykinin may primarily affect layer V neurons in the cat visual cortex.     

Synchronization of intrinsic 0.1‐Hz blood‐oxygen‐level‐dependent oscillations in amygdala and prefrontal cortex in subjects with increased state anxiety

Low‐frequency oscillations with a dominant frequency at 0.1 Hz are one of the most influential intrinsic blood‐oxygen‐level‐dependent (BOLD) signals. This raises the question if vascular BOLD oscillations (originating from blood flow in the brain) and intrinsic slow neural activity fluctuations (neural BOLD oscillations) can be differentiated. In this study, we report on two different approaches: first, on computing the phase‐locking value in the frequency band 0.07–0.13 Hz between heart beat‐to‐beat interval (RRI) and BOLD oscillations and second, between multiple BOLD oscillations (functional connectivity) in four resting states in 23 scanner‐naïve, anxious healthy subjects. The first method revealed that vascular 0.1‐Hz BOLD oscillations preceded those in RRI signals by 1.7 ± 0.6 s and neural BOLD oscillations lagged RRI oscillations by 0.8 ± 0.5 s. Together, vascular BOLD oscillations preceded neural BOLD oscillations by ~90° or ~2.5 s. To verify this discrimination, connectivity patterns of neural and vascular 0.1‐Hz BOLD oscillations were compared in 26 regions involved in processing of emotions. Neural BOLD oscillations revealed significant phase‐coupling between amygdala and medial frontal cortex, while vascular BOLD oscillations showed highly significant phase‐coupling between amygdala and multiple regions in the supply areas of the anterior and medial cerebral arteries. This suggests that not only slow neural and vascular BOLD oscillations can be dissociated but also that two strategies may exist to optimize regulation of anxiety, that is increased functional connectivity between amygdala and medial frontal cortex, and increased cerebral blood flow in amygdala and related structures.     

Concurrently induced plasticity due to convergence of distinct forms of spike timing‐dependent plasticity in the developing barrel cortex

Spike timing‐dependent plasticity (STDP) has been demonstrated in a variety of neural circuits. Recent studies reveal that it plays a fundamental role in the formation and remodeling of neuronal circuits. We show here an interaction of two distinct forms of STDP in the mouse barrel cortex causing concurrent, plastic changes, potentially a novel mechanism underlying network remodeling. We previously demonstrated that during the second postnatal week, when layer four (L4) cells are forming synapses onto L2/3 cells, L4‐L2/3 synapses exhibit STDP with only long‐term potentiation (t‐LTP). We also showed that at the same developmental stage, thalamus‐L2/3 synapses express functional cannabinoid type 1 receptor (CB1R) and exhibit CB1R‐dependent STDP with only long‐term depression (t‐LTD). Thus, distinct forms of STDP with opposite directions (potentiation vs. depression) converge in the target layer of L2/3 during the second postnatal week. As the canonical target layer of the thalamus is L4 and thalamic cells activate both L4 and L2/3 cells, in principle, thalamic activity could induce t‐LTP at L4‐L2/3 and t‐LTD at thalamus‐L2/3 simultaneously. In this study, we tested this possibility. We found that when spike timing stimulation was applied to the thalamus and L2/3 cells, synapses between the thalamus and L2/3 were weakened, whereas synapses between L4 and L2/3 were potentiated; therefore, converging STDP caused the predicted concurrent plasticity. We propose that developmentally transient convergences of STDP may play a role in shaping neural networks by facilitating L4‐L2/3 formation and weakening aberrant thalamic innervation to L2/3, both driven by thalamic activity.     

Immunocytochemical localization of somatostatin and cholecystokinin in the cat visual cortex

Immunocytochemistry was used to examine the morphology and distribution of cholecystokinin-like and somatostatin-like neurons in areas 17, 18 and 19 of cat visual cortex as a function of lamination. Immunoreactive cells of both peptides were observed in all layers of cat visual cortex. While somatostatin-like cells occurred mainly in layers II + III and VI, cholecystokinin-like cells were observed chiefly in the superficial layers (I + II + III). Somatostatin-like cells displayed morphological features of multipolar and bipolar varieties, and cholecystokinin-like cells displayed morphological features of multipolar and bitufted varieties. Similar results were obtained for all 3 areas.     

Immunocytochemical study of GABAA receptors in the cat visual cortex

The laminar distribution and morphological structures associated with GABA_A receptor immunoreactivity in the cat visual cortex were studied by using two different polyclonal antibodies directed either against the purified GABA_A receptor protein (antibody “967”) or against a specific domain of the β₁-subunit of the GABA_A receptor (antibody “Q”). Immunoblots of cat visual cortex tissue with these antibodies revealted that antibody “Q” recognizes only one subunit, namely the β₁-subunit of the GABA_A receptor, and that antibody “967” recognizes three subunits. Both antibodies produced very similar staining patterns, indicating that the β₁-subunit may be an essential component of the GABA_A receptor in the cat visual cortex. The typical staining pattern showed a clear membrane structure around neuronal somata. Using cell body shape criteria, immunopositive neurons included both pyramidal cells in cortical layers II, III, and V, and nonpyramidal cells in all cortical layers. Immunopositive neurons were uniformly distributed in layers II to VI, whereas the density of immunopositive cells in layer I was lower. Some immunopositive neurons were also found in the white matter underlying the visual cotex. In gray matter, immunopositive structures also included dendrites, especially the proximal dendrites, and axon initial segments of pyramidal neurons. The immunopositive processes usually ran vertically toward the pial surface. Some astrocytes were also immunostained. They were localized in layer I and in the white matter. The overall pattern of immunostaining was similar in areas 17, 18, and 19. © 1993 Wiley-Liss, Inc.     

Highly accurate retinotopic maps of the physiological blind spot in human visual cortex

The physiological blind spot is a naturally occurring scotoma corresponding with the optic disc in the retina of each eye. Even during monocular viewing, observers are usually oblivious to the scotoma, in part because the visual system extrapolates information from the surrounding area. Unfortunately, studying this visual field region with neuroimaging has proven difficult, as it occupies only a small part of retinotopic cortex. Here, we used functional magnetic resonance imaging and a novel data‐driven method for mapping the retinotopic organization in and around the blind spot representation in V1. Our approach allowed for highly accurate reconstructions of the extent of an observer’s blind spot, and out‐performed conventional model‐based analyses. This method opens exciting opportunities to study the plasticity of receptive fields after visual field loss, and our data add to evidence suggesting that the neural circuitry responsible for impressions of perceptual completion across the physiological blind spot most likely involves regions of extrastriate cortex—beyond V1.     

Characterization, distribution, and ontogenesis of adenosine binding sites in cat visual cortex

In vitro autoradiographic techniques were used to characterize binding sites for 3H-cyclohexyladenosine (CHA) and 3H-5'-N-ethylcarboxamidoadenosine (NECA) in cat and kitten visual cortex. 3H-CHA binding sites in adult cat have a Bmax of 1,363 fmol/mg protein and a Kd of 6.8 nM. Displacement experiments indicate that 3H-CHA binds to an adenosine receptor similar to the A1-adenosine receptor described by other investigators. 3H-NECA binding sites in adult cat have a Bmax of 518 fmol/mg protein and a Kd of 15.4 nM. Displacement experiments do not allow us to identify this binding site unambiguously. Bmax values increase during postnatal development for both binding sites, peaking in adulthood for 3H-CHA and at 30 d for 3H-NECA. Kd values show neither consistent nor significant differences during postnatal development for either binding site. 3H-CHA and 3H-NECA binding sites are concentrated in layers 1-3 and upper layer 5 in the visual cortex of adult cats. These laminar patterns, however, change during postnatal development, showing the densest binding in the deep cortical layers (5 and 6) in kittens younger than 30 d of age and a fairly homogeneous binding in older kittens before achieving the adult distribution.     

Stimulus‐dependent augmented gamma oscillatory activity between the functionally connected cortical neurons in the primary visual cortex

Neuronal assemblies typically synchronise within the gamma oscillatory band (30–80 Hz) and are fundamental to information processing. Despite numerous investigations, the exact mechanisms and origins of gamma oscillations are yet to be known. Here, through multiunit recordings in the primary visual cortex of cats, we show that the strength of gamma power (20–40 and 60–80 Hz) is significantly stronger between the functionally connected units than between the unconnected units within an assembly. Furthermore, there is increased frequency coherence in the gamma band between the connected units than between the unconnected units. Finally, the higher gamma rhythms (60–80 Hz) are mostly linked to the fast‐spiking neurons. These results led us to postulate that gamma oscillations are intrinsically generated between the connected units within cell assemblies (microcircuits) in relation to the stimulus within an emergent ‘50‐ms temporal window of opportunity’.