Plasticity and tuning of the time course of analog persistent firing in a neural integrator

Abstract

In a companion paper, we reported that the goldfish oculomotor neural integrator could be trained to instability or leak by rotating the visual surround with a velocity proportional to ؉͞؊ horizontal eye position, respectively. Here we analyze changes in the firing rate behavior of neurons in area I in the caudal brainstem, a central component of the oculomotor neural integrator. Persistent firing could be detuned to instability and leak, respectively, along with fixation behavior. Prolonged training could reduce the time constant of persistent firing of some cells by more than an order of magnitude, to <1 s. Normal visual feedback gradually retuned persistent firing of integrator neurons toward stability, along with fixation behavior. In animals with unstable fixations, approximately half of the eye position-related cells had upward or unstable firing rate drift. In animals with leaky fixations, two-thirds of the eye position-related cells showed leaky firing drift. The remaining eye position-related cells, generally those with lower eye position thresholds, showed a more complex pattern of historydependent͞predictive firing rate drift in relation to eye drift. These complex drift cells often showed a drop in maximum persistent firing rate after training to leak. Despite this diversity, firing drift and the degree of instability or leak in firing rates were broadly correlated with fixation performance. The presence, strength, and reversibility of this plasticity demonstrate that, in this system, visual feedback plays a vital role in gradually tuning the time course of persistent neural firing.W e demonstrated in a companion paper (1) how visual feedback with an altered retinal slip vs. eye position gain can be used to detune the goldfish oculomotor neural integrator to extreme instability or leak and how normal visual feedback can retune the integrator to stability. Here we test the hypothesis that visual feedback tunes graded (analog) persistent firing of oculomotor neural integrator neurons themselves.In the vertebrate oculomotor system, the ability to maintain stable eye position depends on the activity of a central ''neural integrator'' responsible for transforming velocity-encoding command or sensory signals to position-encoding outputs that feed into extraocular motoneurons. Experiments in primate (2-6) and cat (7-9) indicate that the velocity-to-position neural integrator (VPNI) for horizontal eye movements is localized in part to two bilateral brainstem nuclei, the nucleus prepositus hypoglossi (NPH) and the medial vestibular nucleus (MVN), reviewed in ref. 10. Experiments in goldfish (11,12) suggest that the horizontal VPNI is localized in part to a bilateral region of the reticulum analogous to the mammalian NPH, termed area I.As shown in Fig. 1a, the spontaneous oculomotor behavior of a control head-fixed goldfish consists of a cyclic scanning pattern of sequential saccades and fixations. With each saccade in the temporal direction of the ipsilateral eye, neurons in area I typically show a brief bur...

Computational Aspects of Feedback in Neural Circuits

“…Another difficult problem in computational neuroscience is to explain how neural circuits can implement a parametric memory, i.e., how they can hold and update an analog value that may represent, for example, an intended eye position that a neural integrator computes from a sequence of eye-movement commands [45], an estimate of elapsed time [9], or accumulated sensory evidence [14]. Various designs have been proposed for parametric memory in recurrent circuits, where continuous attractors (also referred to as line attractors) hold and update an analog value.…”

Spatial Patterns of Persistent Neural Activity Vary with the Behavioral Context of Short-Term Memory

“…If the set of different persistent firing patterns generated by the circuit is sufficiently diverse, then modifications of behavior could be achieved through a relatively simple re-weighting of the contributions made by each firing pattern. In the VPNI, the time constant of oculomotor integration can be modified by visual feedback, a process mediated by the cerebellum (O. Debowy and R. Baker, unpublished observations) that results in changes in the firing of VPNI neurons (Major et al, 2004). The cerebellum could help control the behavioral time constant of integration purely by adjusting the relative strengths of saccadic or optokinetic inputs onto different activity modes in the VPNI.…”

Computational aspects of feedback in neural circuits

“…Another difficult problem in computational neuroscience is to explain how neural circuits can implement a parametric memory, i.e., how they can hold and update an analog value that may represent, for example, an intended eye position that a neural integrator computes from a sequence of eyemovement commands [45], an estimate of elapsed time [9], or accumulated sensory evidence [14]. Various designs have been proposed for parametric memory in recurrent circuits, where continuous attractors (also referred to as line attractors) hold and update an analog value.…”