Neural Mechanisms of Orientation Selectivity in the Visual Cortex

Ferster, David; Miller, Kenneth D.

doi:10.1146/annurev.neuro.23.1.441

Cited by 596 publications

(480 citation statements)

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“…However, we have established here that opposite-polarity Glass patterns drive V1 cells (simple and complex) in a manner that can account for the psychophysical results. Furthermore, it is likely that V1 cells receive both on and off inputs in a push-pull manner (for review, see Ferster and Miller, 2000). Our data and simulations both show that neuronal orientation selectivity is reduced for opposite-polarity Glass patterns.…”

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confidence: 53%

Signals in Macaque Striate Cortical Neurons that Support the Perception of Glass Patterns

Smith¹,

2002

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Glass patterns are texture stimuli made by pairing randomly placed dots with partners at specific offsets. The strong percept of global form that arises from the sparse local orientation cues has made these patterns the subject of psychophysical investigations, yet neuronal responses to Glass patterns have not been studied. We measured the responses of neurons in macaque striate cortex (V1) to dynamic, translational Glass patterns as a function of dot separation and dot-pair orientation. Responses were selective, but were on average more than an order of magnitude weaker than responses to sinusoidal gratings. Response and selectivity were greatest when the dot-pair orientation matched that of the preferred grating and when dot separation was between one-quarter and one-half of the spatial period of the optimal grating; changing the dot-pair separation or inverting the contrast of one of the dots radically changed the orientation selectivity. We computed the expected responses for a receptive field model to translational Glass patterns and found that the complexity of our V1 tuning curves could be understood in terms of the responses of linear filters to pairs of dots. This modeling connects our understanding of V1 receptive fields as rectified, quasi-linear filters with results from psychophysical studies of Glass patterns. Our results provide a basis for studying how subsequent visual areas integrate weak, local signals into global form percepts. Key words: Glass patterns; macaque monkey; primary visual cortex; V1; random dots; orientation selectivity; linear filter; spatial frequencyGlass patterns (Glass, 1969;Glass and Perez, 1973) have been used in numerous psychophysical studies to probe form-detecting mechanisms in human observers (Glass and Switkes, 1976;DeValois and Switkes, 1980;Prazdny, 1984;Earle, 1985;Prazdny, 1986;Dakin, 1997a;Wilson et al., 1997;Wilson and Wilkinson, 1998;Ross et al., 2000;Dakin and Bex, 2001). These patterns are created by taking a "seed" pattern of randomly placed dots and then pairing each dot with another according to a particular geometric rule. The example Glass patterns shown on the left side of Figure 1 were generated by translating, rotating, and magnifying the seed pattern and adding the result back to the original field. The percept of global form in each case is clear, but these global percepts arise purely from the local orientation cues given by pairs of dots. In his first description of these patterns, Glass (1969) speculated on the nature of the cortical responses that they evoked, and proposed that they would be useful for studying the neural basis of form perception. Closely related random-dot stimuli have been used to successfully probe the neuronal mechanisms underlying global coherent percepts in motion processing (Newsome et al., 1989) and depth perception (Poggio et al., 1985).Consideration of the structure of Glass patterns suggests that they are processed in two stages. The first stage must identify local orientation cues in the otherwise random pattern, an...

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confidence: 53%

Signals in Macaque Striate Cortical Neurons that Support the Perception of Glass Patterns

Smith¹,

2002

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“…There has been considerable controversy regarding the degree to which it is the precise arrangement of the ''feedforward'' thalamocortical projections that converge to create orientation tuning in neurons in layer IV of V1. There is now substantial experimental support for some of the aspects of this model ( [24,37,50]; see [25] for a recent review). However, there are also numerous features of orientation tuning that this model cannot explain ( [14,21,44,52]; see [63,65] for a review).…”

Section: Orientation Tuning In Primary Visual Cortexmentioning

confidence: 99%

“…Some models that rely entirely on intracortical connections to produce tuning can produce orientation selectivity without any bias in the thalamocortical input [22]. As the specifics regarding this receptive field transformation are resolved [25,63,65], other issues regarding orientation tuning have begun to emerge into the spotlight.…”

Section: Orientation Tuning In Primary Visual Cortexmentioning

confidence: 99%

“…Given the large number of inputs that any given neuron receives, from a distributed network of neurons, this is not a trivial issue. The percentage of drive provided by thalamocortical inputs is estimated to be roughly a third of the total in simple cells [25]. The rest of the synaptic drive to simple cells derives from the cortex.…”

Section: Generation Vs Maintenance Of Tuningmentioning

confidence: 99%

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Local networks in visual cortex and their influence on neuronal responses and dynamics

Schummers¹,

Mariño²,

Sur³

2004

Journal of Physiology-Paris

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Networks of neurons in the cerebral cortex generate complex outputs that are not simply predicted by their inputs. These emergent responses underlie the function of the cortex. Understanding how cortical networks carry out such transformations requires a description of the responses of individual neurons and of their networks at multiple levels of analysis. We focus on orientation selectivity in primary visual cortex as a model system to understand cortical network computations. Recent experiments in our laboratory and others provide significant insight into how cortical networks generate and maintain orientation selectivity. We first review evidence for the diversity of orientation tuning characteristics in visual cortex. We then describe experiments that combine optical imaging of orientation maps with intracellular and extracellular recordings from individual neurons at known locations in the orientation map. The data indicate that excitatory and inhibitory synaptic inputs are summed across the cortex in a manner that is consistent with simple rules of integration of local inputs. These rules arise from known anatomical projection patterns in visual cortex. We propose that the generation and plasticity of orientation tuning is strongly influenced by local cortical networks-the diversity of these properties arises in part from the diversity of neighbourhood features that derive from the orientation map.

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“…The anatomical substrates for the first two properties (retinotopy and ocular dominance) are the thalamic inputs to layer 4, whereas selectivity for orientation has no established anatomical basis in primates. Unlike cat V1, where it appears that patterned input from the lateral geniculate nucleus to layer 4 provides the basis for orientation selectivity (Hubel and Wiesel, 1962;Ferster and Miller, 2000), neurons in layer 4C of primate V1 are insensitive to stimulus orientation. Instead, sharp orientation tuning is found in layers 2/3 and 4B, one synapse removed from the thalamic input (Hubel and Wiesel, 1968;Dow, 1974;Bullier and Henry, 1980;Blasdel and Fitzpatrick, 1984;Anderson et al, 1993;Ringach et al, 1997).…”

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confidence: 95%

Oriented Axon Projections in Primary Visual Cortex of the Monkey

2001

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One important aspect of the functional architecture of primary visual cortex is the circuitry that accounts for the receptive field properties of neurons. The anatomy that underlies retinotopy and ocular dominance is well known, but no anatomical structure related to orientation selectivity has been found in primates. We examined whether the arrangement of local axon systems projecting within the cortical layers might be correlated with orientation preference in New World monkeys. We found that axons in layer 3 spread out from the site of a tracer injection in an anisotropic manner and that this elongated distribution is aligned with the preferred orientation recorded at each site. Moreover, within a few degrees of the foveal representation, the majority of the axon terminals fall within or just outside of the limits of the cortical mapping of the classical receptive field. Thus local axons produce a field of monosynaptic excitation that aligns with orientation axes and reaches neurons that have receptive fields which are adjacent in visual space.

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Neural Mechanisms of Orientation Selectivity in the Visual Cortex

Cited by 596 publications

References 122 publications

Signals in Macaque Striate Cortical Neurons that Support the Perception of Glass Patterns

Signals in Macaque Striate Cortical Neurons that Support the Perception of Glass Patterns

Local networks in visual cortex and their influence on neuronal responses and dynamics

Oriented Axon Projections in Primary Visual Cortex of the Monkey

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