Spatiotemporal Receptive Field Properties of a Looming-Sensitive Neuron in Solitarious and Gregarious Phases of the Desert Locust

Desert locusts ( Schistocerca gregaria ) can transform reversibly between the swarming gregarious phase and a solitarious phase, which avoids other locusts. This transformation entails dramatic changes in morphology, physiology, and behavior. We have used the lobula giant movement detector (LGMD) and its postsynaptic target, the descending contralateral movement detector (DCMD), which are visual interneurons that detect looming objects, to analyze how differences in the visual ecology of the two phases are served by altered neuronal function. Solitarious locusts had larger eyes and a greater degree of binocular overlap than those of gregarious locusts. The receptive field to looming stimuli had a large central region of nearly equal response spanning 120° × 60° in both phases. The DCMDs of gregarious locusts responded more strongly than solitarious locusts and had a small caudolateral focus of even further sensitivity. More peripherally, the response was reduced in both phases, particularly ventrally, with gregarious locusts showing greater proportional decrease. Gregarious locusts showed less habituation to repeated looming stimuli along the eye equator than did solitarious locusts. By contrast, in other parts of the receptive field the degree of habituation was similar in both phases. The receptive field organization to looming stimuli contrasts strongly with the receptive field organization of the same neurons to nonlooming local-motion stimuli, which show much more pronounced regional variation. The DCMDs of both gregarious and solitarious locusts are able to detect approaching objects from across a wide expanse of visual space, but phase-specific changes in the spatiotemporal receptive field are linked to lifestyle changes.

Inhibitory Contributions to Spatiotemporal Receptive-Field Structure and Direction Selectivity in Simple Cells of Cat Area 17

Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17. Intracortical inhibition contributes to direction selectivity in primary visual cortex, but how it acts has been unclear. We investigated this problem in simple cells of cat area 17 by taking advantage of the link between spatiotemporal (S-T) receptive-field structure and direction selectivity. Most cells in layer 4 have S-T–oriented receptive fields in which gradients of response timing across the field confer a preferred direction of motion. Linear summation of responses across the receptive field, followed by a static nonlinear amplification, has been shown previously to account for directional tuning in layer 4. We tested the hypotheses that inhibition acts by altering S-T structure or the static nonlinearity or both. Drifting and counterphasing sinewave gratings were used to measure direction selectivity and S-T structure, respectively, in 17 layer 4 simple cells before and during iontophoresis of bicuculline methiodide (BMI), a GABAA antagonist. S-T orientation was quantified from fits to response temporal phase versus stimulus spatial phase data. Bicuculline reduced direction selectivity and S-T orientation in nearly all cells, and reductions in the two measures were well correlated ( r = 0.81) and reversible. Using conventional linear predictions based on response phase and amplitude, we found that BMI-induced changes in S-T structure also accounted well for absolute changes in the amplitude and phase of responses to gratings drifting in the preferred and nonpreferred direction. For each cell we also calculated an exponent used to estimate the static nonlinearity. Bicuculline reduced the exponent in most cells, but the changes were not correlated with reductions in direction selectivity. We conclude that GABAA-mediated inhibition influences directional tuning in layer 4 primarily by sculpting S-T receptive-field structure. The source of the inhibition is likely to be other simple cells with certain spatiotemporal relationships to their target. Despite reductions in the two measures, most receptive fields maintained some directional tuning and S-T orientation during BMI. This suggests that their excitatory inputs, arising from the lateral geniculate nucleus and within area 17, are sufficient to create some S-T orientation and that inhibition accentuates it. Finally, BMI also reduced direction selectivity in 8 of 10 simple cells tested in layer 6, but the reductions were not accompanied by systematic changes in S-T structure. This reflects the fact that S-T orientation, as revealed by our first-order measures of the receptive field, is weak there normally. Inhibition likely affects layer 6 cells via more complex, nonlinear interactions.

Strobe Rearing Reduces Direction Selectivity in Area 17 by Altering Spatiotemporal Receptive-Field Structure

Humphrey, Allen L. and Alan B. Saul. Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure. J. Neurophysiol. 80: 2991–3004, 1998. Direction selectivity in simple cells of cat area 17 is linked to spatiotemporal (S-T) receptive-field structure. S-T inseparable receptive fields display gradients of response timing across the receptive field that confer a preferred direction of motion. Receptive fields that are not direction selective lack gradients; they are S-T separable, displaying uniform timing across the field. Here we further examine this link using a developmental paradigm that disrupts direction selectivity. Cats were reared from birth to 8 mo of age in 8-Hz stroboscopic illumination. Direction selectivity in simple cells was then measured using gratings drifting at different temporal frequencies (0.25–16 Hz). S-T structure was assessed using stationary bars presented at different receptive-field positions, with bar luminance being modulated sinusoidally at different temporal frequencies. For each cell, plots of response phase versus bar position were fit by lines to characterize S-T inseparability at each temporal frequency. Strobe rearing produced a profound loss of direction selectivity at all temporal frequencies; only 10% of cells were selective compared with 80% in normal cats. The few remaining directional cells were selective over a narrower than normal range of temporal frequencies and exhibited weaker than normal direction selectivity. Importantly, the directional loss was accompanied by a virtual elimination of S-T inseparability. Nearly all cells were S-T separable, like nondirectional cells in normal cats. The loss was clearest in layer 4. Normally, inseparability is greatest there, and it correlates well ( r = 0.77) with direction selectivity; strobe rearing reduced inseparability and direction selectivity to very low values. The few remaining directional cells were inseparable. In layer 6 of normal cats, most direction-selective cells are only weakly inseparable, and there is no consistent relationship between the two measures. However, after strobe rearing, even the weak inseparability was eliminated along with direction selectivity. The correlated changes in S-T structure and direction selectivity were confirmed using conventional linear predictions of directional tuning based on responses to counterphasing bars and white noise stimuli. The developmental changes were permanent, being observed up to 12 yr after strobe rearing. The deficits were remarkably specific; strobe rearing did not affect spatial receptive-field structure, orientation selectivity, spatial or temporal frequency tuning, or general responsiveness to visual stimuli. These results provide further support for a critical role of S-T structure in determining direction selectivity in simple cells. Strobe rearing eliminates directional tuning by altering the timing of responses within the receptive field.

Temporal diversity in the lateral geniculate nucleus of cat

Reverse correlation was used in conjunction with ternary white noise to estimate the first-order spatiotemporal receptive-field structure of LGN cells in the anesthetized, paralyzed cat. Based on a singular-value decomposition of these data, we conclude that most LGN cells are approximately space–time separable. An analysis of the timecourses of the first singular values revealed a strongly bimodal but continuous distribution of rise times and waveforms. The two modes represented cells generally associated with the lagged and nonlagged classes of Mastronarde (1987a,b), and this was confirmed by their responses to step and sine-modulated spots in their field centers. The intermediate cells, rather than appearing to constitute a separate group, smoothly filled the region between the obviously lagged and nonlagged cells in every respect. These conclusions are limited to X-cells although the data from a much smaller population of Y-cells conform to the same scheme. We conclude that lagged and nonlagged cells represent the modes of a continuous and very broad distribution of temporal responses in the cat LGN.