Abstract

’Gain-field-like’ tuning behavior is characterized by a modulation of the neuronal response depending on a certain variable, without changing the actual receptive field characteristics in relation to another variable. Eye position gain fields were first observed in area 7a of the posterior parietal cortex (PPC), where visually responsive neurons are modulated by ocular position. Analysis of artificial neural networks has shown that this type of tuning function might comprise the neuronal substrate for coordinate transformations. In this work, neuronal activity in the dorsal medial superior temporal area (MSTd) has been analyzed with an focus on it’s involvement in oculomotor control. MSTd is part of the extrastriate visual cortex and located in the PPC. Lesion studies suggested a participation of this cortical area in the control of eye movements. Inactivation of MSTd severely impairs the optokinetic response (OKR), which is an reflex-like kind of eye movement that compensates for motion of the whole visual scene. Using a novel, information-theory based approach for neuronal data analysis, we were able to identify those visual and eye movement related signals which were most correlated to the mean rate of spiking activity in MSTd neurons during optokinetic stimulation. In a majority of neurons firing rate was non-linearly related to a combination of retinal image velocity and eye velocity. The observed neuronal latency relative to these signals is in line with a system-level model of OKR, where an efference copy of the motor command signal is used to generate an internal estimate of the head-centered stimulus velocity signal. Tuning functions were obtained by using a probabilistic approach. In most MSTd neurons these functions exhibited gain-field-like shapes, with eye velocity modulating the visual response in a multiplicative manner. Population analysis revealed a large diversity of tuning forms including asymmetric and non-separable functions. The distribution of gain fields was almost identical to the predictions from a neural network model trained to perform the summation of image and eye velocity. These findings therefore strongly support the hypothesis of MSTd’s participation in the OKR control system by implementing the transformation from retinal image velocity to an estimate of stimulus velocity. In this sense, eye velocity gain fields constitute an intermediate step in transforming the eye-centered to a head-centered visual motion signal.Another aspect that was addressed in this work was the comparison of the irregularity of MSTd spiking activity during optokinetic response with the behavior during pure visual stimulation. The goal of this study was an evaluation of potential neuronal mechanisms underlying the observed gain field behavior. We found that both inter- and intra-trial variability were decreased with increasing retinal image velocity, but increased with eye velocity. This observation argues against a symmetrical integration of driving and modulating inputs. Instead, we propose an architecture where multiplicative gain modulation is achieved by simultaneous increase of excitatory and inhibitory background synaptic input. A conductance-based single-compartment model neuron was able to reproduce realistic gain modulation and the observed stimulus-dependence of neural variability, at the same time. In summary, this work leads to improved knowledge about MSTd’s role in visuomotor transformation by analyzing various functional and mechanistic aspects of eye velocity gain fields on a systems-, network-, and neuronal level.