An Analysis of Primate Inhibitory Burst Neuron Spike Trains using System
Identification Techniques: III. Relationship to Motor-Error during Head-Fixed
Saccades and Head-free Gaze Shifts.
Kathleen E. Cullen and Daniel Guitton.
Aerospace Medical Research Unit and the Montreal Neurological Institute,
McGill University, Montreal, Quebec H3G 1Y6, Canada.
APStracts 4:180N, 1997.
ABSTRACT
The classic model of saccade generation assumes that the burst generator is
driven by a motor-error signal = the difference between the actual eye
position and the final, "desired", eye position in the orbit. Here we evaluate
objectively, using system identification techniques, the dynamic relationship
between motor-error signals and primate IBN discharges (upstream analysis).
The IBNs presented here are the same neurons whose downstream relationships
were characterized during head-fixed saccades and head-free gaze shifts in our
companion papers. In our analysis of head-fixed saccades, we determined how
well IBN discharges encode eye motor-error (ee) compared to downstream
saccadic eye movement dynamics; and whether long lead IBN (LLIBNs) discharges
encode ee better than short lead IBN (SLIBNs) given that it is commonly
assumed that short lead burst neurons are closer than long lead burst neurons
to the motor output and thus further from the ee signal. In the ee based
models tested, IBN firing frequency, B(t), was represented by either: (model
1u), a non-linear function of ee; (model 2u), a linear function of ee
B(t)=rk+ a1ee(t)] where the bias term, rk, was estimated separately for each
saccade; (model 3u), a version of 2u wherein the bias term was a function of
saccade amplitude; and (4u) a linear function of ee with an added pole term
(the derivative of firing rate). Models based on ee consistently produced
worse predictions of IBN activity than models of comparable complexity based
on eye movement dynamics (eg. eye velocity). Hence, the simple two parameter
downstream model 2d [B(t)=r+b1E(t)(] was much better than any upstream (ee-
based) model with a comparable number of parameters. The link between B(t) and
ee is due primarily to the correlation between the declining phases of B(t)
and ee: motor-error models did not predict well the rising phase of the
discharge. We could improve substantially the performance of upstream models
by adding an ee( term. Since ee(= -E(, this was equivalent to incorporating E(
terms into upstream models which erased the distinction between upstream and
downstream analyses. Adding an ee( term to the upstream models made them as
good as downstream ones in predicting B(t). However the ee term now became
redundant since its removal did not affect model accuracy. Thus when E( is
available as a parameter, ee becomes irrelevant. In the head-free monkey the
ability of upstream models to predict IBN firing during head-free gaze shifts
when gaze, eye, or head motor-error signals were model inputs, was poor and
similar to the upstream analysis of the head-fixed condition. We conclude,
that during saccades (head-fixed) or gaze shifts (head-free) the activity of
both SLIBNs and LLIBNs is more closely linked to downstream events (i.e. the
dynamics of ongoing movements) than to the coincident upstream motor-error
signal. Furthermore SLIBNs and LLIBNs do not differ in their characteristics:
the latter are not, as is usually hypothesized, closer to a motor-error signal
than the former.
Received 13 August 1997; accepted in final form 2 July 1997.
APS Manuscript Number J650-6.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1997 The American Physiological Society.
Published in APStracts on 28 August 1997