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Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex.

Direction selectivity in simple cells of primary visual cortex, defined from their spike responses, cannot be predicted using linear models. It has been suggested that the shunting inhibition evoked by visual stimulation is responsible for the nonlinear component of direction selectivity. Cortical inhibition would suppress a neuron's firing when stimuli move in the nonpreferred direction, but would allow responses to stimuli in the preferred direction. Models of direction selectivity based solely on input from the lateral geniculate nucleus, however, propose that the nonlinear response is caused by spike threshold. By extracting excitatory and inhibitory components of synaptic inputs from intracellular records obtained in vivo, we demonstrate that excitation and inhibition are tuned for the same direction, but differ in relative timing. Further, membrane potential responses combine in a linear fashion. Spike threshold, however, quantitatively accounts for the nonlinear component of direction selectivity, amplifying the direction selectivity of spike output relative to that of synaptic inputs.

Action Potentials↗

Processing of first-order motion in marmoset visual cortex is influenced by second-order motion.

We measured the responses of single neurons in marmoset visual cortex (V1, V2, and the third visual complex) to moving first-order stimuli and to combined first- and second-order stimuli in order to determine whether first-order motion processing was influenced by second-order motion. Beat stimuli were made by summing two gratings of similar spatial frequency, one of which was static and the other was moving. The beat is the product of a moving sinusoidal carrier (first-order motion) and a moving low-frequency contrast envelope (second-order motion). We compared responses to moving first-order gratings alone with responses to beat patterns with first-order and second-order motion in the same direction as each other, or in opposite directions to each other in order to distinguish first-order and second-order direction-selective responses. In the majority (72%, 67/93) of cells (V1 73%, 45/62; V2 70%, 16/23; third visual complex 75%, 6/8), responses to first-order motion were significantly influenced by the addition of a second-order signal. The second-order envelope was more influential when moving in the opposite direction to the first-order stimulus, reducing first-order direction sensitivity in V1, V2, and the third visual complex. We interpret these results as showing that first-order motion processing through early visual cortex is not separate from second-order motion processing; suggesting that both motion signals are processed by the same system.

Action Potentials↗

Ultrastructure of synapses and golgi analysis of neurons in neocortex of the lateral gyrus (visual cortex) of the dolphin and pilot whale.

Qualitative and computerized quantitative analyses of ultrastructural features of synapses in different layers of the primary visual cortex in the dolphin (Stenella coeruleoalba) and the pilot whale (Globicephala melaena) were carried out. Also, Golgi and cytoarchitectonic analyses were performed in the same species of cetaceans and, additionally, in Tursiops truncatus and Phocaena phocaena. It was found that on a synaptic level, as well as in cytoarchitectonic and Golgi features, the neocortex of cetaceans combines evolutionary progressive features and conservative features with a marked prevalence of the latter. Thus, the total number of synapses in visual neocortex in cetaceans is closer to this value in higher Primates. On the other hand, the laminar density of synapses per mm3 is generally the same in all layers in cetacean visual cortex and numerically is close to values found in small lissencephalic brains. Also, the synapse/neuron ratio in the dolphin visual cortex is of the same order as in cortices of rodents and lagomorphs and much higher than in cortices of advanced terrestrial mammals. Layers I and II contain approximately 70% of the total synapses in the cortical slab through visual cortex. Layer I also contains the extraverted dendrites of neurons of layer II and thus these two layers resemble a paleoarchicortical type of organization superimposed on a more typical neocortical organization of the lower cortical layers. In this respect the convexity neocortex of cetaceans is generally similar to the neocortices of phylogenetically ancient extant mammals such as basal Insectivora and Chiroptera.

Animals↗

Functional hyperemic response in the rat visual cortex under halothane anesthesia.

To establish a model for functional hyperemia in the rat visual cortex, cortical blood flow responses to flash stimulation were measured with the laser Doppler flow (LDF) technique at various levels of halothane anesthesia. The concentration-dependent effect of halothane on arterial pressure and its consequent effect on the hyperemic response were also investigated. Using a stroboscopic light source, 10 flashes at 1 min intervals were delivered to the left eye of 12 Sprague-Dawley rats. LDF responses were measured bilaterally in the monocular primary visual cortex (V1M) at steady state halothane concentrations between 0.4 and 1.4%. In six rats, methoxamine (MX) was infused to prevent halothane-induced hypotension; the remaining rats did not receive MX. In all rats, LDF response to flash commenced within 1s and peaked at 2.5s in the contralateral V1M, but not in ipsilateral V1M. The maximum LDF response was 25% at 0.5% halothane and 12% at 1.4% halothane. In rats without MX infusion, mean arterial pressure (MAP) fell from 138 to 90 mmHg when halothane increased from 0.4 to 1.4%. MX infusion prevented the hypotension, but did not influence the LDF response, suggesting that the halothane's effect was direct rather than pressure-mediated. We demonstrate for the first time, a robust functional hyperemic response to discrete flash stimuli in the primary visual cortex of halothane-anesthetized albino rats that can be measured with LDF over a wide range of halothane concentrations and is not fully suppressed at surgical levels of halothane anesthesia.

Anesthetics, Inhalation↗

Development of phorbol ester (protein kinase C) binding sites in cat visual cortex.

Tritiated phorbol-12,13-dibutyrate [( 3H]PDBu), a phorbol ester, was utilized to autoradiographically localize protein kinase C (PKC) in the cat visual cortex. Thin, slide-mounted sections of adult cat brain were used to characterize binding of [3H]PDBu. This was found to be saturable, reversible, and more readily displaced by phorbol ester than by synthetic diacylglycerols. Binding sites displayed a tissue concentration of 20 pmol/mg protein, and a dissociation constant of 8.0 nM. [3H]PDBu was slow to associate with its receptor, requiring 9.5 h to reach equilibrium. Autoradiograph revealed that PKC is heterogeneously distributed in the cat brain, and displays a laminar-specific pattern in the visual cortex. This laminar distribution undergoes marked changes during the first two months of postnatal life. In the visual cortex of neonatal kittens, [3H]PDBu binding is confined to layers I and V. Layer III acquires high levels of binding by postnatal day 15, layer II by 28 days, and layer VI becomes labelled by 40 days of age. Adult animals exhibit high levels of binding in all laminae except layer IV. Age-dependent changes in PKC's laminar distribution do not seem to be correlated with specific anatomical, neurochemical, or behavioural events during development. PKC appears to be associated with cell bodies or processes intrinsic to the visual cortex, and is probably not located on the terminals of cortical afferents.

Aging↗

Abnormal visual cortex development in the kitten associated with maternal dietary taurine deprivation.

We have examined the visual cortex of newborn and 8-week-old kittens born to mothers consuming a taurine-supplemented or taurine-free diet using the rapid Golgi technique. Kittens from taurine-supplemented mothers exhibited normal development of the visual cortex. Kittens from taurine-depleted mothers showed striking differences. In newborn kittens, neuroblasts are aggregated both at the ventricular and pial zones, having failed to migrate and differentiate normally. Eight weeks after birth, only few pyramidal and nonpyramidal neurons are found. Those present have heavily spined dendritic processes indicative of poor arborization. Protoplasmic astrocytes are represented by undifferentiated cellular masses. The taurine concentration in the cortex of such kittens is four- to fivefold smaller than in kittens from taurine-supplemented mothers. These results suggest that normal concentrations of taurine in visual cortex, as well as cerebellum, are required for normal ontogeny of neurons. Once such deficits are established in the prenatal and immediate postnatal period, they result in permanent abnormalities. These findings have clear implications for vegetarian women who intend to have children, since virtually no taurine is present in plants and vegetables.

Aging↗

Preservation of functional architecture in visual cortex of cats with experimentally induced hydrocephalus.

We investigated how neural function is preserved or matured in the visual cortex of cats, following the induction of hydrocephalus by kaolin injection. In vivo optical imaging of intrinsic signals in 11-17-week-old hydrocephalic cats revealed orientation maps showing the orderly arrangement of preferred orientations when stimulated by grating stimuli at a low spatial frequency, whereas stimulus-evoked intrinsic signals in response to gratings at a high spatial frequency were often too weak to construct orientation maps. Furthermore, in two of the three hydrocephalic cats, initially deteriorated orientation maps became almost regular maps in the second imaging experiments conducted 8 and 11 weeks, respectively, after the first imaging. This indicates that, despite large structural deformation of the hydrocephalic brain, orientation maps are elaborated sufficiently after the age of 5-6 months, by which time the orientation map formation is usually completed in normal cats. Single unit recording from the decompressed visual cortex revealed that many neurons showed normal orientation selectivity, whereas the binocularity of these neurons was found to be reduced. These results suggested that the deformed visual cortex of hydrocephalic cats exhibits a high plasticity, retaining its functional organization.

Action Potentials↗

[Lateralization of opioid receptors and their putative ligands in the visual cortex of the turtle].

Opioid mu-agonist morphine, delta-agonist D-Ala2,D-Leu5-enkephalin (DADL) and kappa-agonist bremazocine locally applied to the surface of turtle visual cortex inhibited the orthodromic evoked potential (EP; fast negative component N1). The lack of cross-desensitization to the inhibitory action of opioids upon EP indicates that the drugs exert their effects via different opioid receptors. Morphine and bremazocine predominantly inhibited the left cortex EP, whereas DADL was a potent inhibitor of the right cortex EP. Thus opioid receptors which modulate evoked electrical activity of the left visual cortex (LVC) apparently belong mostly to mu- and kappa-type while delta-receptors were predominantly responsible for the modulation of electrical activity in the right visual cortex (RVC). Application of LVC- and RVC-extracts to the cortex surface led to EP inhibition, which was partially (60-80%) prevented by antagonist naloxone. LVC-extract proved to be a more potent inhibitor of the left cortex EP, whereas RVC-extract was found to be more effective when applied to the right cortex. It is suggested that not only opioid receptors, but also their endogenous ligands are lateralized in turtle visual cortex.

Animals↗

Retinal constraints on orientation specificity in cat visual cortex.

Most retinal ganglion cells (Levick and Thibos, 1982) and cortical cells (Leventhal, 1983; Leventhal et al., 1984) subserving peripheral vision respond best to stimuli that are oriented radially, i.e., like the spokes of a wheel with the area centralis at the hub. We have extended this work by comparing directly the distributions of orientations represented in topographically corresponding regions of retina and visual cortex. Both central and peripheral regions were studied. The relations between the orientations of neighboring ganglion cells and the manner in which the overrepresentation of radial orientations is accommodated in the functional architecture of visual cortex were also studied. Our results are based on an analysis of the orientations of the dendritic fields of 1296 ganglion cells throughout the retina and the preferred orientations of 1389 cells located in retinotopically corresponding regions of cortical areas 17, 18, and 19 in the cat. We find that horizontal and vertical orientations are overrepresented in regions of both retina and visual cortex subserving the central 5 degrees of vision. The distributions of the orientations of retinal ganglion cells and cortical cells subserving the horizontal, vertical, and diagonal meridians outside the area centralis differ significantly. The distribution of the preferred orientations of the S (simple) cells in areas 17, 18 and 19 subserving a given part of the retina corresponds to the distribution of the dendritic field orientations of the ganglion cells in that part of retina. The distribution of the preferred orientations of C (complex) cells with narrow receptive fields in area 17 but not C cells with wide receptive fields in areas 17, 18, or 19 subserving a given part of the retina matches the distribution of the orientations of the ganglion cells in that part of retina. The orientations of all of the alpha-cells in 5-9 mm2 patches of retina along the horizontal, vertical, and oblique meridians were determined. A comparison of the orientations of neighboring cells indicates that other than a mutual tendency to be oriented radially, ganglion cells with similar orientations are not clustered in the retina. Reconstructions of electrode penetrations into regions of visual cortex representing peripheral retina indicate that columns subserving radial orientations are wider than those subserving nonradial orientations. Our results provide evidence that the distribution of the preferred orientations of simple cells in visual cortex subserving any region of the visual field matches the distribution of the orientations of the ganglion cells subserving the same region of the visual field.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Benzodiazepine ([3H]flunitrazepam) binding in cat visual cortex: ontogenesis of normal characteristics and the effects of dark rearing.

[3H]Flunitrazepam (FNZ) binding sites were characterized in homogenates of cat visual cortex during normal postnatal development and following dark rearing from birth. In parallel experiments, the distribution and density of [3H]FNZ binding sites were examined by in vitro autoradiographic or 'scrape' methods. In homogenates, Bmax measurements showed low early values, rising to a peak in receptor density at about 60 days postnatal, followed by a decline in adulthood. At all ages, gamma-aminobutyric acid (GABA) altered the Kd, but not the Bmax of [3H]FNZ binding sites. Kd values showed a general increase with age, parallelled by an increased sensitivity to GABA. Receptor autoradiography revealed that the highest density of [3H]FNZ binding sites was in layer IV of cats of all ages. Deafferentation of extrinsic inputs to the visual cortex by surgical undercutting did not alter this pattern of laminar distribution, indicating that the receptors were associated with intrinsic cortical elements rather than subcortical inputs. Dark rearing had no effect on [3H]FNZ laminar distribution in the visual cortex. The Bmax was higher at 30 days postnatal, but did not differ significantly thereafter. Modulation by GABA was concomitantly higher at 30 days, but lower than normal in dark-reared animals at ages greater than 30 days postnatal. The results are discussed in relation to the normal and abnormal development of GABA receptors in the cat visual cortex.

Animals↗

Differential effect of dark rearing on long-term potentiation induced by layer IV and white matter stimulation in rat visual cortex.

In the earlier work, we showed that primed-burst stimulation (PBs) is an effective protocol to induce long-term potentiation (LTP) in layer II/III of adult rat visual cortex in vitro. In the present study, we investigated effects of dark rearing on potentiation of layer II/III responses to stimulation of layer IV or the underlying white matter in the visual cortex in vitro. Long-term potentiation was induced by PBs applied to white matter or layer IV of the cortex in light and dark reared rats. Regardless of the stimulation site, layer II/III field potentials consisted of two components. In general, the latency of responses in dark reared rats was shorter than that in light reared ones. Whereas PBs of layer IV produced LTP of two components in both the groups, that of white matter induced an appreciable potentiation of the second component in both groups and the first component only in dark reared rats. These results indicate that PBs of either white matter or layer IV can gain access to the modifiable synapses that are related to the second component of layer II/III responses in light and dark reared visual cortex, but accessibility of the modifiable synapses that are related to first component depends on the tetanization site. The dark rearing enhances accessibility of the modifiable synapses that are related to the first component following PBs of the white matter. It is suggested that the immaturity of inhibitory circuits and/or better function of excitatory ones in the visual cortex of dark reared rats may contribute to the enhanced accessibility of the first component.

Animals↗

Interlaminar connections of the visual cortex in the hedgehog (Paraechinus hypomelas).

The contribution of each cortical lamina to intracortical circuitry was studied in the visual neocortex of the Pakistani hedgehog. Punctate laminar lesions were made electrolytically within the visual cortex, and after five to seven days the brains were processed and stained with the Fink-Heimer technique. The results of this study suggest that both horizontal and vertical connections are important to the organization of visual cortex in the hedgehog. The horizontal projections originate at three distinct cortical depths. Lesions in layer II reveal projections that traverse the inner one-half of layer I; lesions in layers III and IV reveal projections that traverse layer IV and that enter the cortical white matter; lesions in layers V and VI reveal projections that traverse the outer one-half of layer VI and that enter the cortical white matter. The vertical projections are oriented perpendicular to the pial surface. Layers II and III project to underlying layer V. Layers V and VI in turn contribute to a reciprocal projection back to all superficial cortical laminae. This anatomical data about intracortical circuitry is discussed with reference to the functional organization of visual cortex.

Animals↗

Reticular suppression of flash-evoked IPSPs in visual cortex neurons.

In a majority of visual cortex (VC) neurons recorded intracellularly in chronically implanted rabbits, light flashes evoked responses consisting of protracted IPSPs (duration 160-200 msec) followed in some cases by a rebound. Inhibition of spontaneous activity through high frequency reticular stimulation (MRF) or through presentations of non-visual arousing stimuli, was not associated with strong hyperpolarization of the cell membrane. Reticular stimulation evoking both activation and inhibition of spontaneous neuronal activity elicited attenuation or complete elimination elimination (disinhibition) of flash-evoked protracted IPSPs and of the postinhibitory rebounds. Rhythmic neuronal discharges elicited by stimulation of the visual pathway was also reduced during reticular activation, due to attenuation of the IPSP-rebound sequence.

Animals↗

TrkB-like immunoreactivity is present on geniculocortical afferents in layer IV of kitten primary visual cortex.

Exogenous administration of the neurotrophins brain-derived neurotrophic factor (BDNF) or neurotrophin-4/5 (NT-4/5), or blockade of their endogenous actions, have been reported to affect the anatomic organization and physiological responses of neurons in developing mammalian primary visual cortex. Experimental alteration of levels of these neurotrophic factors can also influence the morphology of the geniculocortical afferents that project from the lateral geniculate nucleus (LGN) to primary visual cortex. BDNF and NT-4/5 are ligands of the TrkB tyrosine kinase receptor. Although multiple populations of cortical neurons express TrkB, it is not known whether geniculocortical afferents express this receptor on their axon branches in visual cortex. We have anatomically labeled geniculocortical afferents of postnatal day 40 kittens with the anterograde neuronal tracer Phaseolus vulgaris leucoagglutinin (PHA-L) and performed double-label immunofluorescence with a panel of anti-TrkB antibodies. Confocal microscopy and object-based colocalization analysis were used to measure levels of TrkB-like immunoreactivity (IR) on geniculocortical afferents in layer IV of primary visual cortex. By using a conservative analysis involving a comparison of measured colocalization with the amount of colocalization expected based on random overlap of TrkB puncta and PHA-L--labeled afferents, 3 of 5 anti-TrkB antibodies tested showed significant colocalization with the geniculocortical axons. Results for the other two antibodies were indeterminate. The indices obtained for colocalization of TrkB and geniculocortical afferents were also compared with the equivalent index obtained for GAD65, a protein that has a similar overall expression pattern to that of TrkB but is not expressed on geniculocortical axons. This analysis indicated that TrkB was present on geniculocortical axons for all five TrkB antibodies tested. TrkB-like IR was also observed on neuronal somata in the LGN. These results indicate that TrkB receptors on geniculocortical afferents are potential mediators of the actions of BDNF and NT-4/5 in developing visual cortex.

Animals↗

Identification and localization of 5-hydroxytryptamine receptor sites in macaque visual cortex.

The two main receptor subtypes for 5-hydroxytryptamine (5HT) were measured and localized in visual cortical areas of macaque monkey. [3H]5HT was used to label all 5HT-1 receptor subtypes and [3H]ketanserin was used to label 5HT-2 receptors. Both receptor types could be demonstrated in membranes prepared from macaque primary visual cortex. The specificity of these ligands for 5HT-1 or 5HT-2 receptors was demonstrated by the pharmacological profile of inhibitors of the specific binding. 5HT-1A receptor sites were detected by displacement experiments and by direct labeling with [3H]8-hydroxy-2(di-n-propylamino) tetralin 8OH-DPAT. Receptor autoradiography showed that the distribution of these receptor subtypes varied from one part of visual cortex to another. 5HT-1 receptors, labeled with [3H]5HT were present in several bands through layer IV of primary visual cortex with the densest band seen in and above layer IVA: another band was in lower layer VI. The band in layer VI was predominantly 5HT-1A sites. There were two main bands of 5HT-2 receptor sites, the most prominent around the IV/V boundary, and the other extending from layer IVA upwards. Adjacent areas showed 5HT receptors in a broad band corresponding to layer IV. 5HT-1A sites were found in superficial layers of adjacent areas, except V2. These layering patterns did not correspond precisely with cytoarchitectonic layering, nor with the pattern of 5HT-containing presynaptic fibres in published reports. It is important, therefore, in considering the role of the 5HT-containing neurons in cortical function to take account not only of the anatomy of the presynaptic terminals, but also of the postsynaptic receptors upon which the released transmitter will act, and their location within the cortex.

8-Hydroxy-2-(di-n-propylamino)tetralin↗

Figure-ground activity in primary visual cortex is suppressed by anesthesia.

By means of their small receptive fields (RFs), neurons in primary visual cortex perform highly localized analyses of the visual scene, far removed from our normal unified experience of vision. Local image elements coded by the RF are put into more global context, however, by means of modulation of the responses of the V1 neurons. Contextual modulation has been shown to follow closely the perceptual interpretation of the scene as a whole. This would suggest that some aspects of contextual modulation can be recorded only in awake and perceiving animals. In this study, multi-unit activity was recorded with implanted electrodes from primary visual cortex of awake, fixating monkeys viewing textured displays in which figure and ground regions were segregated by differences in either orientation or motion. Contextual modulation was isolated from local RF processing, by keeping RF stimulation identical across trials while sampling responses for various positions of the RF relative to figure and ground. Contextual modulation was observed to unfold spatially and temporally in a way that closely resembles the figure-ground percept. When recording was repeated, but with the animals anesthetized, the figure-ground related modulatory activity was selectively suppressed. RF tuning properties, however, remained unaffected. The results show that the modulatory activity is functionally distinct from the RF properties. V1 thus hosts distinct regimes of activity that are mediated by separate mechanisms and that depend differentially on the animal being awake or anesthetized.

Anesthesia, Inhalation↗

Functional connectivity between somatosensory and visual cortex in early blind humans.

Crossmodal plasticity occurs when loss of input in one sensory modality leads to reorganization in brain representations of other sensory modalities. In congenital blindness the visual cortex becomes responsive to somatosensory input such as occurs during Braille reading. The route by which somatosensory information reaches the visual cortex is not known. Here, we used repetitive transcranial magnetic stimulation (rTMS) to probe the connection between primary somatosensory cortex (S1) and early visual cortex (V1 and neighboring areas), combining rTMS with positron emission tomography (PET). We applied stimulation over S1 in sighted, early blind and late blind individuals. Baseline regional cerebral blood flow in occipital cortex was highest in early blind and lowest in late blind individuals. Only the early blind group showed significant activation of early visual areas when rTMS was delivered over S1. This activation was significantly higher in early than in late blind, but not relative to sighted controls. These results are consistent with the hypothesis that tactile information may reach early visual areas in early blind humans through cortico-cortical pathways, possibly supporting enhanced tactile information processing.

Age of Onset↗

Optical imaging of epileptiform events in visual cortex in response to patterned photic stimulation.

In a subset of patients with epilepsy, patterned visual stimuli can trigger clinical seizures. The etiology of this phenomenon, and the complex interaction between functional architecture and epilepsy, were investigated in ferret visual cortex. Optical imaging of intrinsic signals was used to visualize maps of orientation, ocular dominance and spatial frequency. Acute interictal spike foci were then induced within V1 using focal iontophoresis of bicuculline methiodide and optically mapped during presentation of patterned visual stimuli. We found that specific orientations and spatial frequencies could preferentially trigger epileptiform events, depending on the location of the epicenter of the epileptic focus within the columnar architecture of visual cortex. These data support a cortical etiology of the clinical phenomenon of pattern-sensitive epilepsy. We were not able to demonstrate a spatial correlation between the functional architecture maps and the topography of the epileptic focus. These findings implicate short-range rather than long-range horizontal excitatory connections in the lateral spread of interictal spikes, which may be specific to the epilepsy model of acute focal disinhibition. Orientation and spatial frequency maps were severely disturbed in the region of the focus but were unaltered in the surrounding cortex. Thus, optical imaging of intrinsic signals can be used to simultaneously map epilepsy and normal functional anatomy with high spatial resolution.

Action Potentials↗