Local and large-range inhibition in feature detection

Abstract

Lateral inhibition is perhaps the most ubiquitous of neuronal mechanisms, having been demonstrated in early stages of processing in many different sensory pathways of both mammals and invertebrates. Recent work challenges the long-standing view that assumes that similar mechanisms operate to tune neuronal responses to higher order properties. Scant evidence for lateral inhibition exists beyond the level of the most peripheral stages of visual processing, leading to suggestions that many features of the tuning of higher order visual neurons can be accounted for by the receptive field and other intrinsic coding properties of visual neurons. Using insect target neurons as a model, we present unequivocal evidence that feature tuning is shaped not by intrinsic properties but by potent spatial lateral inhibition operating well beyond the first stages of visual processing. In addition, we present evidence for a second form of higher-order spatial inhibition--a long-range interocular transfer of information that we argue serves a role in establishing interocular rivalry and thus potentially a neural substrate for directing attention to single targets in the presence of distracters. In so doing, we demonstrate not just one, but two levels of spatial inhibition acting beyond the level of peripheral processing.

Figure 1.

The receptive field of CSTMD1. A, A receptive field map of a CSTMD1 neuron recorded in the left hemisphere. The map shows responses to a 0.9 × 0.9° dark target drifting at 55°/s from left to right, color coded to indicate the spike frequency. The spiking response is calculated as the average frequency within 100 ms bins. B, A receptive field map of the same CSTMD1 when the target drifted right to left. C, A receptive field map when the target drifted upward. D, The receptive field for a target drifted downward. E, A schematic of the morphology of CSTMD1. The cell body is located contralateral to our recording site. The dendrites in the protocerebrum in this hemisphere are not beaded. There are two beaded output regions in the left hemisphere—one in the protocerebrum and one covering the expanse of the lobula. CB, Cell body; Med, medulla; Lob, lobula; Ch, inner optic chiasm; Prot, protocerebrum; SOG, subesophageal ganglion; L, lateral; D, dorsal; M, medial; V, ventral.

Figure 2.

Model schematic of input to CSTMD1. Prefiltered inputs (white triangles) from the right eye are pooled via local spatial summation into ESTMDs. The ESTMDs are tuned to small targets via a combination of lateral inhibition (black triangles) and fast temporal adaptation (not shown). Many ESTMDs synapse onto an STMD in the lobula, which in turn synapses onto CSTMD1 (solid lines) in the protocerebrum. CSTMD1 inhibits its mirror counterpart (dashed lines) in the contralateral protocerebrum. A second large output region in the lobula has an unknown function (synapses depicted with gray triangles).

Figure 3.

Local spatial inhibition. A, Raw spiking response to a single 0.9 × 0.9° target drifting at 55°/s from left to right. B, The response of the same neuron is attenuated when a distracter target is added at 3.5° separation (measured center to center). C, The response is restored when the two targets are separated by 9°. The long bar beneath the trace indicates the peristimulus duration (2 s) of the primary target (solid line) and distracter target (dashed line), and the short bar indicates the 200 ms (11°) analysis window. D, Pooled data across neurons [mean (N) ± SEM; N = 8, n = 38; except for separations of 9, 6.3, 4.5, and 2.7°, N = 6; 18°, N = 5; 1.8°, N = 3]. Responses were determined by averaging the spike rates within a 200 ms analysis window (indicated in C). In each trial, the distracter target was separated vertically from the primary target as indicated by the x-axis (distances measured center to center). Negative values indicate that the distracter target drifted below the primary target; positive values indicate that it drifted above (see pictogram). At a separation of 0°, the distracter target overlaid the primary target, thereby creating a single control. The spontaneous rate is shown by the dashed line. The asterisks indicate significance (p < 0.05) compared with the control (paired t test).

Figure 4.

Interocular interactions. A, Spike histogram (N = 1, n = 4, average spike rate within 50 ms bins) showing the response to a single 0.9 × 0.9° target drifting at 55°/s from left to right. B, The response is reduced with the addition of a second target drifting with a 3.5° separation (measured center to center). The solid black bar beneath the histogram represents the peristimulus duration of the primary target. The gray dashed line indicates the peristimulus duration of the distracter target. Separations were calculated as the triangulated distance between the two target centers (using the Pythagorean theorem). C, When the targets are separated by 19°, the response to the primary target remains suppressed as the distracter target drifts through the left visual field. D, The response is still reduced when the targets are separated by 43°. The short bar indicates the 200 ms (11°) analysis window. E, Pooled data across neurons [mean (N) ± SEM; N = 3, n = 11]. Responses were determined by averaging the spike rate within the 200 ms analysis window (indicated in D). The spontaneous rate is shown by the dashed line.

Figure 5.

Large-range interocular inhibition. A, Spiking response to a single 0.9 × 0.9° target drifting upward shown in 50 ms bins. B, The response is reduced with the addition of a distracter target drifting at a separation of 3.5°. C, The response is restored when the two targets drift at 9° separation. D, In this neuron, the response to the two targets is inhibited below spontaneous rate when the distracter target drifts in the left visual field at −36° separation. The peristimulus duration of the primary target (solid line) and distracter target (dashed line) are indicated beneath the histogram; the short bar indicates the 200 ms (11°) analysis window. E, Pooled data across neurons [mean (N) ± SEM; N = 7, n = 26; except for separations of 36, 27, 3.6°, N = 6; 54, 21.6, 6.3°, N = 5; 2.7, 1.8°, N = 3]. Negative x-axis values indicate that the distracter target drifted to the left of the primary target; positive values indicate that it drifted to the right (see pictogram, with the midline shown with a dashed line). The spontaneous rate is shown by the dashed line. The asterisks indicate significance (p < 0.05) compared with the control (paired t test). F, Pooled data for a 0.8 s (40°) analysis window below the hot spot for the same dataset as E. The spontaneous rate is shown by the dashed line.

Figure 6.

Directional interocular inhibition. A, Spike histogram (average spike rate in 50 ms bins) showing the response to a single target (see pictogram) drifting vertically upward 14° to the right of the midline (N = 1; n = 24). The targets were timed so that the primary target drifted through location A at the same time as the distracter target drifted through its mirror location B. B, The response is inhibited when a distracter target moving in the same direction is added. The peristimulus duration of the primary target is indicated by the solid black bar, and the distracter target by the dashed gray bar. C, The response when the distracter target drifts to the left. D, The response is marginally suppressed when the distracter target drifts from top to bottom. E, There is a mild suppression when the distracter target drifts from left to right. The short bar indicates the 200 ms (11°) analysis window, with the corresponding location shown in each pictogram as a small dashed box. F, Pooled data for the response corresponding to the direction of the distracter target [mean (n) ± SEM; N = 1, n = 24]. The arrows beneath the graph indicate the direction of the distracter (gray/dashed). The solid black arrow indicates the response to a single target (control from A). The dashed line shows the spontaneous rate. G, Direction selectivity for the same neuron to a single target drifting in four directions [mean (n) ± SEM; N = 1, n = 3]. The arrows beneath the graph indicate the direction of travel. Data were analyzed for a target drifting in four directions through location A. The dashed line shows the spontaneous rate.

Figure 7.

Local inhibition of a single ESTMD. A, The schematic diagram shows the inhibitory response generated by a distracter target. Responses to the distracter target (data from Figs. 3, 5) drifting at varying separations from the primary target were averaged to give a single value, which was assigned a grayscale level. The outer boundary of each circular region corresponds to the separation between the two targets. Two targets at a separation of 1.8° are shown for comparison. B, The ommatidial mosaic of the dorsal acute zone of H. tau with interreceptor angles of 0.56° (Horridge, 1978). The outlined region (below) corresponds to the central disc in A, drawn at the same scale.

Figure 8.

High-resolution local inhibition. A, Responses [mean (n) ± SEM; N = 1, n = 4] when two targets drifting horizontally were separated vertically. At a separation of 0°, the distracter target overlaid the primary target, thereby creating a single control. The spontaneous rate is shown by the dashed line. B, The illustration shows the scale of two targets separated by 1.8° on the ommatidial mosaic. In this case, the responses are above control level (single target; see A), but should be readily resolvable by the optics of the dragonfly eye. C, When targets are separated by 2.7°, the data show complete suppression of responses even though the targets are separated by approximately five ommatidia (measured center–center).