Selectivity For Stimulus Orientation Research Articles

Functional characterization and spatial clustering of visual cortical neurons in the predatory grasshopper mouse Onychomys arenicola.

Mammalian neocortical circuits are functionally organized such that the selectivity of individual neurons systematically shifts across the cortical surface, forming a continuous map. Maps of the sensory space exist in cortex, such as retinotopic maps in the visual system or tonotopic maps in the auditory system, but other functional response properties also may be similarly organized. For example, many carnivores and primates possess a map for orientation selectivity in primary visual cortex (V1), whereas mice, rabbits, and the gray squirrel lack orientation maps. In this report we show that a carnivorous rodent with predatory behaviors, the grasshopper mouse (Onychomys arenicola), lacks a canonical columnar organization of orientation preference in V1; however, neighboring neurons within 50 μm exhibit related tuning preference. Using a combination of two-photon microscopy and extracellular electrophysiology, we demonstrate that the functional organization of visual cortical neurons in the grasshopper mouse is largely the same as in the C57/BL6 laboratory mouse. We also find similarity in the selectivity for stimulus orientation, direction, and spatial frequency. Our results suggest that the properties of V1 neurons across rodent species are largely conserved.NEW & NOTEWORTHY Carnivores and primates possess a map for orientation selectivity in primary visual cortex (V1), whereas rodents and lagomorphs lack this organization. We examine, for the first time, V1 of a wild carnivorous rodent with predatory behaviors, the grasshopper mouse (Onychomys arenicola). We demonstrate the cellular organization of V1 in the grasshopper mouse is largely the same as the C57/BL6 laboratory mouse, suggesting that V1 neuron properties across rodent species are largely conserved.

Melting the Iceberg: Contrast Invariance in Visual Cortex

Neurons in visual cortex maintain their selectivity for stimulus orientation despite wide variations in stimulus contrast. Achieving this invariance is a challenge because of the iceberg effect: subthreshold responses are broader in selectivity than firing responses, and increasing contrast would bring them above threshold. An article in this issue of Neuron by Finn et al. explains how neurons solve this problem using simple mechanisms: contrast-gain control, additive noise, and firing threshold.

Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex

Neurons in the cerebral cortex are organized into anatomical columns, with ensembles of cells arranged from the surface to the white matter. Within a column, neurons often share functional properties, such as selectivity for stimulus orientation; columns with distinct properties, such as different preferred orientations, tile the cortical surface in orderly patterns. This functional architecture was discovered with the relatively sparse sampling of microelectrode recordings. Optical imaging of membrane voltage or metabolic activity elucidated the overall geometry of functional maps, but is averaged over many cells (resolution >100 microm). Consequently, the purity of functional domains and the precision of the borders between them could not be resolved. Here, we labelled thousands of neurons of the visual cortex with a calcium-sensitive indicator in vivo. We then imaged the activity of neuronal populations at single-cell resolution with two-photon microscopy up to a depth of 400 microm. In rat primary visual cortex, neurons had robust orientation selectivity but there was no discernible local structure; neighbouring neurons often responded to different orientations. In area 18 of cat visual cortex, functional maps were organized at a fine scale. Neurons with opposite preferences for stimulus direction were segregated with extraordinary spatial precision in three dimensions, with columnar borders one to two cells wide. These results indicate that cortical maps can be built with single-cell precision.

Dark-reared cats: responsitivity of cortical cells influenced pharmacologically by an inhibitory antagonist.

When studied physiologically, dark-reared kittens exhibit abnormal responses. Specifically, cortical cells respond poorly, if at all, to visual stimulation. In the preceding paper (Ramoa et al. 1986) we showed that iontophoretic application of an excitatory amino acid allows all cells in this preparation to be excited or suppressed by visual stimuli. In the current study, we have pursued this finding by studying additional dark-reared kittens using iontophoretic application of an inhibitory antagonist, bicuculline methiodide (BIC). Responses of most cells studied were affected by application of BIC. Of cells which were originally weak or unresponsive, 76% became clearly responsive with application of BIC. Of cells which responded without BIC and were orientation-selective, only 33% lost selectivity during application of BIC. Considered together, these findings suggest functional inhibitory input in dark-reared animals which appears to differ from that in normal kittens with respect to its role in selectivity for stimulus orientation.

Central core control of developmental plasticity in the kitten visual cortex: I. Diencephalic lesions.

In five, dark-reared, 4-week-old kittens the posterior two thirds of the corpus callosum were split, and a lesion comprising the intralaminar nuclei was made of the left medial thalamic complex. In addition, the right eye was closed by suture. Post-operatively, the kittens showed abnormal orienting responses, neglecting visual stimuli presented in the hemifield contralateral to the side of the lesion. Sudden changes in light, sound, or somatosensory stimulation elicited orienting responses that all tended toward the side of the lesion. These massive symptoms faded within a few weeks but the kittens continued to neglect visual stimuli in the hemifield contralateral to the lesion when a second stimulus was presented simultaneously in the other hemifield. Electrophysiologic analysis of the visual cortex, performed after the end of the critical period, revealed marked interhemispheric differences. In the visual cortex of the normal hemisphere most neurons were monocular and responded exclusively to stimulation of the open eye, but otherwise had normal receptive field properties. In the visual cortex of the hemisphere containing the thalamic lesion, the majority of the neurons remained binocular. In addition, the selectivity for stimulus orientation and the vigor of responses to optimally aligned stimuli were subnormal on this side. Thus, the same retinal signals, which in the control hemisphere suppressed the pathways from the deprived eye and supported the development of normal receptive fields, failed to do either in the hemisphere containing the thalamic lesion. Apparently, experience-dependent changes in the visual cortex require both retinal stimulation and the functioning of diencephalic structures which modulate cortical excitability and control selective attention.

Rabbit visual cortical neurons with simple and complex receptive fields

Receptive fields of neurons of the rabbit visual cortex selective for stimulus orientation were investigated. These receptive fields were less well differentiated than those of the analogous neurons of the cat visual cortex (large in size and circular in shape). Two mechanisms of selectivity for stimulus orientation were observed: inhibition between on and off zones of the receptive field (sample type) and oriented lateral inhibition within the same zone of the receptive field (complex type). Lateral inhibition within the same zone of the receptive field also took place in unselective neurons; "complex" selective neurons differed from them in the orientation of this inhibition. A combination of both mechanisms was possible in the receptive field of the same neuron. It is suggested that both simple and complex receptive fields are derivatives of unselective receptive fields and that "complex" neurons are not the basis for a higher level of analysis of visual information than in "simple" neurons.

Quantitative study of cortical orientation selectivity in visually inexperienced kitten.

1. Extracellular recordings were made from single units in the visual cortices of six kittens deprived of experience with pattern vision by binocular lid suture. 2. Selectivity for stimulus orientation was quantitatively assessed in 98 units; 90 responded selectively to the orientation of a moving bar stimulus, the remainder responding nonselectively or too poorly to classify. Cells in these visually inexperienced kittens were similar in their degree of selectivity for orientation to cells tested in adult cats. However, responses tended to be weaker and somewhat more erratic. 3. About half the cells in this simple responded to both directions of stimulus motion at the optimal orientation. Most of those responding to only one direction of motion were considered orientation rather than direction selective because they responded more strongly or more selectively to a moving bar than to a moving spot. 4. Cells appeared to be organized within the cortex in a pattern similar to that found in adult cats, with cells in one column selective for the same orientation, and adjacent column having similar preferred orientations. 5. It is concluded that selectivity for stimulus orientation in the cat's visual cortex is innately determined.