Neuronal responses in the cortical area MSTd during smooth pursuit and ocular following eye movements

Abstract

The motion sensitive medial superior temporal (MST) area has been implicated in a variety of functions such as smooth pursuit (SP) generation, self-motion perception, and coding of visual target motion. For self-motion perception, the dorsal part of MST (MSTd) is crucial [1], e.g., neurons in MSTd respond to optic flow simulating selfmotion. However, about 35% of MSTd neurons also respond to smooth pursuit eye movements, which is difficult to reconcile in the context of self-motion perception. Here, we examined neuronal responses of 55 pursuit-sensitive MSTd neurons recorded in two awake macaque monkeys [2], and related these responses to a computational model of the smooth pursuit system [3].Four stimulus conditions were applied: 1) step-ramp SP in response to a moving laser spot (5-20°/s), 2) target blanking (duration 100 ms) during SP, 3) ocular following response to moving visual large-field (LF) stimuli (5-20°/s), 4) visual perturbation (5 Hz sinusoid, ±10°/s) of target or LF motion [2]. Most neurons (n = 49) also responded during LF stimuli, but with different characteristics: 1) the preferred direction for LF was opposite to that of SP, and 2) for LF stimuli, neuronal responses preceded eye movement onset by 34.1 ms, but lagged behind eye movement onset during SP by 128 ms. Target blanking led to a transient decrease in eye velocity, but not to a change in neural responses (n = 22). Perturbations during LF motion or SP consistently caused changes in eye velocity. However, while 93% of the tested neurons (n = 15) responded to LF perturbations, only 33% (of 55) responded during SP. Again, neuronal perturbation responses preceded changes in eye movement for LF, but lagged behind eye movement for SP.For model simulations, we extended our non-linear pursuit model [3] by appropriate temporal delays. The MSTbranch of the model contains an eye-movement related signal, which lags behind the eye by about the same amount as the eye lags behind target motion (120-135 ms vs. 128 ms neuronal delay). This signal, constituting a delayed efferent copy signal, is used to reconstruct target motion in space [4]. Being extra-retinal in origin, it also persists during target blanking, consistent with our data. However, even though these characteristics are in accordance with our model, the major differences between neuronal LF and SP responses despite similar eye movements suggest a different explanation, compatible with earlier findings [5]: if LF motion is interpreted as being caused by self-motion in space, pursuit-sensitive neurons in MSTd would code for gaze velocity in world-centered coordinates.

The Response of MSTd Neurons to Perturbations in Target Motion During Ongoing Smooth-Pursuit Eye Movements

“…Interestingly, this neuronal delay (127 ms) and the delay of pursuit onset with respect to target motion (120 -140 ms) exhibit similar values. The similarity of temporal delays together with simulations of our nonlinear pursuit model incorporating delays (Brostek et al 2009) suggest that the extraretinal pursuit signal of MSTd neurons may serve to reconstruct target velocity in space, which then could be represented in MSTl, as suggested previously (Ilg and Thier 2003). The representation of the perturbation response in our MSTd neurons is compatible with this idea, since it reflects what was predicted from our modeling of the step-ramp responses.…”