Persistent Firing and Adaptation in Optic Flow Sensitive Descending Neurons

Sarah Nicholas,Karin Nordström

doi:10.2139/ssrn.3552149

Abstract

A general principle of sensory systems is that they adapt to prolonged stimulation by reducing their response over time. Indeed, many visual systems, including higher-order motion sensitive neurons in the fly optic lobes and the mammalian visual cortex, a reduction in neural activity following prolonged stimulation occurs. In contrast to this phenomenon, the response of the motor system controlling flight maneuvers persists following the offset of visual motion. It has been suggested that this gap is caused by a lingering calcium signal in the output synapses of optic lobe neurons. However, whether this directly affects the responses of the post-synaptic descending neurons, leading to the observed behavioral output, is not known. We use extracellular electrophysiology to record from optic flow sensitive descending neurons in response to prolonged wide-field stimulation. We find that, as opposed to most sensory and visual neurons, and in particular to the motion vision sensitive neurons in the brains of flies and mammals, the descending neurons show little adaption during stimulus motion. In addition, we find that the optic flow sensitive descending neurons display persistent firing, or an after-effect, following the cessation of visual stimulation, consistent with the lingering calcium signal hypothesis. However, if the difference in after-effect is compensated for, subsequent presentation of stimuli in a test-adapt-test paradigm reveals adaptation to visual motion. Our results thus show an interesting combination of adaptation and persistent firing, in the neurons that project to the thoracic ganglia, and thereby control behavioral output.

Highlights

Sensory systems typically adapt to prolonged stimulation by reducing their response over time
Descending Neurons Show Limited Adaptation When optic-flow-sensitive descending neurons in the hoverfly are stimulated for 1 s with a full-contrast, full-screen, preferred-direction sinusoidal grating (Figure 1A), they respond with vigorous firing, as seen in the raw data from an optic-flowsensitive type 2 neuron (Figure 1B, dashed lines indicate peristimulus duration)
There is little or no adaptation to 1 s of continuous motion across temporal frequencies (Figures 1C and 1D), and even an increase in response to 0.5 Hz stimulation in the type 2 neuron (Figure 1D). This is strikingly different to what is seen in the pre-synaptic lobula plate tangential cells (LPTCs), which adapt strongly to continuous motion stimulation, especially at higher temporal frequencies [22, 38, 39]

Summary

Introduction

Sensory systems typically adapt to prolonged stimulation by reducing their response over time. Sensory adaptation is an active, stimulus specific process, separate from neural fatigue [2, 5, 6]. Neurons in many other cortical and subcortical areas show persistent neural activity following a brief sensory stimulus, lasting from hundreds of milliseconds to tens of seconds (for Review, see [7, 8]). Post-stimulus persistent firing of pre-motor neurons in the velocity-to-position neural integrator maintains oculomotor fixation [9, 10] and is used for sensory short-term memory [11]. Persistent firing is common in areas with local feedback loops, including the superior colliculus [12], posterior parietal cortex [13], and spinal cord [14, 15]

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Conclusion