Role of spike-frequency adaptation in shaping neuronal response to dynamic stimuli

Spike-frequency adaptation is the reduction of a neuron’s firing rate to a stimulus of constant intensity. In the locust, the Lobula Giant Movement Detector (LGMD) is a visual interneuron that exhibits rapid adaptation to both current injection and visual stimuli. Here, a reduced compartmental model of the LGMD is employed to explore adaptation’s role in selectivity for stimuli whose intensity changes with time. We show that supralinearly increasing current injection stimuli are best at driving a high spike count in the response, while linearly increasing current injection stimuli (i.e., ramps) are best at attaining large firing rate changes in an adapting neuron. This result is extended with in vivo experiments showing that the LGMD’s response to translating stimuli having a supralinear velocity profile is larger than the response to constant or linearly increasing velocity translation. Furthermore, we show that the LGMD’s preference for approaching versus receding stimuli can partly be accounted for by adaptation. Finally, we show that the LGMD’s adaptation mechanism appears well tuned to minimize sensitivity for the level of basal input. This article is part of a special issue on Neuronal Dynamics of Sensory Coding.     

Responses of descending neurons to looming stimuli in the praying mantis <Emphasis Type="Italic">Tenodera aridifolia</Emphasis>

Responses to visual stimuli of some neurons that descend the nerve cord from the brain were recorded extracellularly in the mantis Tenodera aridifolia. Most of the recorded neurons showed their largest responses to looming stimuli that simulated a black circle approaching towards the mantis. The neurons showed a transient excitatory response to a gradually darkening or receding circle. The neurons showed sustained excitation to the linearly expanding stimuli, but the spike frequency decreased rapidly. The responses of the neurons were affected by both the diameter and the speed of looming stimuli. Faster or smaller looming stimuli elicited a higher peak frequency. These responses were observed in both recordings from the connective between suboesophageal and prothoracic ganglia and the connective between prothoracic and mesothoracic ganglia. There was a one-to-one correspondence of spike firing between these two recordings with a fixed delay. The neurons had the receptive field on ipsilateral side to its axon at the cervical connective. These results suggest that there is a looming-sensitive descending neuron, with an axon projecting over prothoracic ganglion, in the mantis nervous system.     

Gliding behaviour elicited by lateral looming stimuli in flying locusts

We challenged tethered, flying locusts with visual stimuli looming from the side towards one eye in a way that mimics the approach of a predatory bird. Locusts respond to the lateral approach of a looming object with steering movements and a stereotyped, rapid behaviour in which the wingbeat pattern ceases and the wings are swept into a gliding posture. This gliding behaviour may cause the locust to dive. The gliding posture is maintained for 200 ms or more after which flight is resumed with an increased wingbeat frequency or else the wings are folded. A glide begins with a strong burst of activity in the mesothoracic second tergosternal motor neuron (no. 84) on both sides of the locust. Recordings of descending contralateral movement detector (DCMD) activity in a flying locust show that it responds to small (80-mm diameter) looming stimuli during tethered flight, with a prolonged burst of spikes that tracks stimulus approach and reaches peak instantaneous frequencies as, or after, stimulus motion ceases. There is a close match between the visual stimuli that elicit a gliding behaviour and those that are effective at exciting the DCMD neuron. Wing elevation into the gliding posture occurs during a maintained burst of high frequency DCMD spikes.     

Discharge patterns of locust visual interneurones

The spike discharges of the descending contralateral movement detector (DCMD) neurone, and of some smaller visual interneurones (S-units), were recorded in the ventral nerve cord of adult Schistocerca gregaria Forsk., in response to a stationary disc (25^o) or a small spot (0.2^o) stimulus. The discharge rate of each neurone was plotted over a period of 5 s exposure; the total number of spikes in this period was also noted. The DCMD response to the 25^o disc was a high-frequency burst falling off quickly to a low rate; the 0.2^o spot evoked a prolonged discharge with an early peak in rate. In S-units the discharge was prolonged with both targets; the rate rose to an early peak in each case, with a much higher rate for the larger disc. For the DCMD the total number of spikes per stimulus (5 s) was greater for the 0.2^o spot; for S-units it was greater for the 25^o disc. Thus an increase of about 30-fold in the number of ommatidia stimulated resulted in a fall in the total DCMD response to about one-quarter; a similar increase evoked a rise of about 6-fold in the S-unit response. When the 25^o disc was presented at progressively reduced intensities the total spike response of the DCMD rose steadily to a maximum at about 2.9 μ W m^-2; using the same procedure the spike output of S-units, initially high, declined monotonically. The role of inhibition in these results is discussed.     

Preparing for escape: an examination of the role of the DCMD neuron in locust escape jumps

Many animals begin to escape by moving away from a threat the instant it is detected. However, the escape jumps of locusts take several hundred milliseconds to produce and the locust must therefore be prepared for escape before the jumping movement can be triggered. In this study we investigate a locust’s preparations to escape a looming stimulus and concurrent spiking activity in its pair of uniquely identifiable looming-detector neurons (the descending contralateral movement detectors; DCMDs). We find that hindleg flexion in preparation for a jump occurs at the same time as high frequency DCMD spikes. However, spikes in a DCMD are not necessary for triggering hindleg flexion, since this hindleg flexion still occurs when the connective containing a DCMD axon is severed or in response to stimuli that cause no high frequency DCMD spikes. Such severing of the connective containing a DCMD axon does, however, increase the variability in flexion timing. We therefore propose that the DCMD contributes to hindleg flexion in preparation for an escape jump, but that its activity affects only flexion timing and is not necessary for the occurrence of hindleg flexion.