Analysis of primate IBN spike trains using system identification techniques. II. Relationship to gaze, eye, and head movement dynamics during head-free gaze shifts

We have investigated the relationships among the firing frequency B(t) of inhibitory burst neurons (IBNs) and the metrics and dynamics of the eye, head, and gaze (eye + head) movements generated during voluntary combined eye-head gaze shifts in monkey. The same IBNs were characterized during head- fixed saccades in our first of three companion papers. In head-free gaze shifts, the number of spikes (NOS) in a burst was, for 82% of the neurons, better correlated with gaze amplitude than with the amplitude of either the eye or head components of the gaze shift. A multiple regression analysis confirmed that NOS was well correlated to the sum of head and eye amplitudes during head-free gaze shifts. Furthermore, the mean slope of the relationship between NOS and gaze amplitude was significantly less for head-free gaze shifts than for head-fixed saccades. NOS is a global parameter. To refine we used system identification techniques to evaluate a series of dynamic models in which IBN spike trains were related to gaze or eye movements. We found that gaze- and eye-based models predicted the discharges of IBNs equally well. However, the bias values required by gaze-based models were comparable to those required in our head-fixed models whereas those required by eye- based models were significantly larger. The difference in biases between gaze- and eye-based models was very strongly correlated to the mean head velocity (Ḣ) during gaze shifts [R = -0.93 ± 0.15 (SD)]. This result suggested that the increased bias required by the eye-based models reflected an unmodeled Ḣ input onto these cells. To pursue this argument further we investigated a series of dynamic models that included both eye velocity (Ė) and Ḣ terms and this confirmed the importance of these two terms. As in our head-fixed analysis of companion paper I, the most valuable model formulation also included an eye saccade amplitude term (ΔE) and was given by B(t) = r₀ + r₁ΔE + b:1Ė + g₁Ḣ where r₀, r₁, b₁, and g₁ are constants. The amplitude of the head velocity coefficient was significantly less than that of the eye velocity coefficient. Furthermore, in our population long-lead IBNs tended to have a smaller head velocity coefficients than short-lead IBNs. We conclude that during head-free gaze shift, the head velocity signal carried to the abducens nucleus by primate excitatory burst neurons (EBNs; if EBNs and IBNs carry similar signals) must be offset by other premotor cells.