Constraints on the Source of Short-Term Motion Adaptation in Macaque Area MT. I. The Role of Input and Intrinsic Mechanisms

Abstract

Neurons in area MT, a motion-sensitive area of extrastriate cortex, respond to a step of target velocity with a transient-sustained firing pattern. The transition from a high initial firing rate to a lower sustained rate occurs over a time course of 20–80 ms and is considered a form of short-term adaptation. The present paper asks whether adaptation is due to input-specific mechanisms such as short-term synaptic depression or if it results from intrinsic cellular mechanisms such as spike-rate adaptation. We assessed the contribution of input-specific mechanisms by using a condition/test paradigm to measure the spatial scale of adaptation. Conditioning and test stimuli were placed within MT receptive fields but were spatially segregated so that the two stimuli would activate different populations of inputs from the primary visual cortex (V1). Conditioning motion at one visual location caused a reduction of the transient firing to subsequent test motion at a second location. The adaptation field, estimated as the region of visual space where conditioning motion caused adaptation, was always larger than the MT receptive field. Use of the same stimulus configuration while recording from direction-selective neurons in V1 failed to demonstrate either adaptation or the transient-sustained response pattern that is the signature of short-term adaptation in MT. We conclude that the shift from transient to sustained firing in MT cells does not result from an input-specific mechanism applied to inputs from V1 because it operates over a wider range of the visual field than is covered by receptive fields of V1 neurons. We used a direct analysis of MT neuron spike trains for many repetitions of the same motion stimulus to assess the contribution to adaptation of intrinsic cellular mechanisms related to spiking. On a trial-by-trial basis, there was no correlation between number of spikes in the transient interval and the interval immediately after the transient period. This is opposite the prediction that there should be a correlation if spikes cause adaptation directly. Further, the transient was suppressed or extinguished, not delayed, in trials in which the neuron emitted zero spikes during the interval that showed a transient in average firing rate. We conclude that the transition from transient to sustained firing in neurons in area MT is caused by mechanisms that are neither input-specific nor controlled by the spiking of the adapting neuron. We propose that the short-term adaptation observed in area MT emerges from the intracortical circuit within MT.