A general function of cerebral cortex is to allow the flexible association of sensory stimuli with specific behaviours. Many neurons in parietal, prefrontal and motor cortical areas are activated both by particular movements and by sensory cues that trigger these movements, suggesting a role in linking sensation to action. For example, neurons in the lateral intraparietal area (LIP) encode both the location of visual stimuli and the direction of saccadic eye movements. LIP is not believed to encode non-spatial stimulus attributes such as colour. Here we investigated whether LIP would encode colour if colour was behaviourally linked to the eye movement. We trained monkeys to make an eye movement in one of two directions based alternately on the colour or location of a visual cue. When cue colour was relevant for directing eye movement, we found a substantial fraction of LIP neurons selective for cue colour. However, when cue location was relevant, colour selectivity was virtually absent in LIP. These results demonstrate that selectivity of cortical neurons can change as a function of the required behaviour.
Neurons in the primary visual cortex of the cat are selectively activated by stimuli with particular orientations. This selectivity can be disrupted by the application of antagonists of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA) to a local region of the cortex. In order to determine whether inhibitory inputs are necessary for a single cortical neuron to show orientation selectivity, GABA receptors were blocked intracellularly during whole cell recording. Although the membrane potential, spontaneous activity, subfield antagonism, and directional selectivity of neurons were altered after they were perfused internally with the blocking solution, 18 out of 18 neurons remained selective for stimulus orientation. These results indicate that excitatory inputs are sufficient to generate orientation selectivity.
In mammalian neocortex, the orderly arrangement of columns of neurons is thought to be a fundamental organizing principle. In primary visual cortex (V1), neurons respond preferentially to bars of a particular orientation, and, in many mammals, these orientationselective cells are arranged in a semiregular, smoothly varying map across the cortical surface. Curiously, orientation maps have not been found in rodents or lagomorphs. To explore whether this lack of organization in previously studied rodents could be attributable to low visual acuity, poorly differentiated visual brain areas, or small absolute V1 size, we examined V1 organization of a larger, highly visual rodent, the gray squirrel. Using intrinsic signal optical imaging and single-cell recordings, we found no evidence of an orientation map, suggesting that formation of orientation maps depends on mechanisms not found in rodents. We did find robust orientation tuning of single cells, and this tuning was invariant to stimulus contrast. Therefore, it seems unlikely that orientation maps are important for orientation tuning or its contrast invariance in V1. In vertical electrode penetrations, we found little evidence for columnar organization of orientation-selective neurons and little evidence for local anisotropy of orientation preferences. We conclude that an orderly and columnar arrangement of functional response properties is not a universal characteristic of cortical architecture.
Integration of inputs by cortical neurons provides the basis for the complex information processing performed in the cerebral cortex. Here, we have examined how primary visual cortical neurons integrate classical and nonclassical receptive field inputs. The effect of nonclassical receptive field stimuli and, correspondingly, of long-range intracortical inputs is known to be context-dependent: the same long-range stimulus can either facilitate or suppress responses, depending on the level of local activation. By constructing a large-scale model of primary visual cortex, we demonstrate that this effect can be understood in terms of the local cortical circuitry. Each receptive field position contributes both excitatory and inhibitory inputs; however, the inhibitory inputs have greater influence when overall receptive field drive is greater. This mechanism also explains contrast-dependent modulations within the classical receptive field, which similarly switch between excitatory and inhibitory. In order to simplify analysis and to explain the fundamental mechanisms of the model, self-contained modules that capture nonlinear local circuit interactions are constructed. This work supports the notion that receptive field integration is the result of local processing within small groups of neurons rather than in single neurons.
We recorded from parietal neurons in monkeys (Macacca mulatta) trained to report the direction of an apparent motion stimulus consisting of regularly spaced columns of dots surrounded by an aperture. Displacing the dots by half their inter-column spacing produced vivid apparent motion that could be perceived in either the preferred or anti-preferred direction for each neuron. Many neurons in the lateral intraparietal area (LIP) responded more strongly on trials in which the animals reported perceiving the neurons' preferred direction, independent of the hand movement used to report their percept. This selectivity was less common in the medial superior temporal area (MST) and virtually absent in the middle temporal area (MT). Variations in activity of LIP and MST neurons just before motion onset were also predictive of the animals' subsequent perceived direction. These data suggest a hierarchy of representation in parietal cortex, whereby neuronal responses become more aligned with subjective perception in higher parietal areas.
Neurons in primary visual cortex (area 17) respond vigorously to oriented stimuli within their receptive fields; however, stimuli presented outside the suprathreshold receptive field can also influence their responses. Here we describe a fundamental feature of the spatial interaction between suprathreshold center and subthreshold surround. By optical imaging of intrinsic signals in area 17 in response to a stimulus border, we show that a given stimulus generates activity primarily in iso-orientation domains, which extend for several millimeters across the cortical surface in a manner consistent with the architecture of long-range horizontal connections in area 17. By mapping the receptive fields of single neurons and imaging responses from the same cortex to stimuli that include or exclude the aggregate suprathreshold receptive field, we show that intrinsic signals strongly reveal the subthreshold surround contribution. Optical imaging and single-unit recording both demonstrate that the relative contrast of center and surround stimuli regulates whether surround interactions are facilitative or suppressive: the same surround stimulus facilitates responses when center contrast is low, but suppresses responses when center contrast is high. Such spatial interactions in area 17 are ideally suited to contribute to phenomena commonly regarded as part of "higher-level" visual processing, such as perceptual "popout" and "filling-in."A prominent feature of nearly every region of the mammalian cortex is a dense network of patchy, long-range horizontal connections within the superficial cortical layers (1). In primary visual cortex, these connections arise primarily as axonal branches of pyramidal cells in layers 2/3 (2, 3), and link neurons located at distances up to several millimeters away in the superficial cortical layers. Long-range horizontal connections make excitatory synapses on their target neurons (4), but those postsynaptic neurons can be excitatory (spiny stellate or pyramidal cells) or inhibitory (smooth stellate cells, see ref. 5).Although these anatomical features of horizontal connections are by now well established, their physiological role remains only partially understood. Long-range connections in area 17 are clustered into regions with similar orientation preference (6), and form a likely substrate for mediating influences on neurons from outside their "classical" receptive field. (We define the classical receptive field as the region over which a stimulus can evoke a suprathreshold spike response from the cell.) These influences can include modulation of orientation specific responses in area 17 neurons (7,8). Consistent with the anatomy of long-range connections, the effect of electrically stimulating lateral connections in cortical slices can be both excitatory and inhibitory, although the balance between the two can be modified (9). Reducing thalamocortical excitation, either in the long term by a retinal lesion (10) or in the short term by an artificial scotoma (11,12), causes changes in ...
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