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Guy Major

Publications and source records attributed to Guy Major.

7 recordsLinked to original sources
PubMed2004

Plasticity and tuning by visual feedback of the stability of a neural integrator.

Persistent neural firing is of fundamental importance to working memory and other brain functions because it allows information to be held "online" following an input and to be integrated over time. Many models of persistent activity rely on some kind of positive feedback internal to the neural circuit concerned; however, too much feedback causes runaway firing (instability), and too little results in loss of persistence (leak). This parameter sensitivity leads to the hypothesis that the brain uses an error signal (external feedback) to tune the stability of persistent firing by adjusting the amount of internal feedback. We test this hypothesis by manipulating external visual feedback, a putative sensory error signal, in a model system for persistent firing, the goldfish oculomotor neural integrator. Over tens of minutes to hours, electronically controlled visual feedback consistent with a leaky or unstable integrator can drive the integrator progressively more unstable or leaky, respectively. Eye fixation time constants can be reduced >100-fold to <1 s. Normal visual feedback gradually retunes the integrator back to stability. Changes in the phase of the sinusoidal vestibulo-ocular response are consistent with integrator detuning, as are changes in ocular drift following eye position shifts compensating for brief passive head movements during fixations. Corresponding changes in persistent firing of integrator neurons are presented in the accompanying article. The presence, strength, and reversibility of the plasticity demonstrate that, in this system, external visual feedback plays a vital role in gradually tuning the stability of the neural integrator.

Animals↗
PubMed2004

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

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 history-dependent/predictive 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.

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PubMed2004

Persistent neural activity: prevalence and mechanisms.

Persistent neural activity refers to a sustained change in action potential discharge that long outlasts a stimulus. It is found in a diverse set of brain regions and organisms and several in vitro systems, suggesting that it can be considered a universal form of circuit dynamics that can be used as a mechanism for short-term storage and accumulation of sensory or motor information. Both single cell and network mechanisms are likely to co-operate in generating persistent activity in many brain areas.

Action Potentials↗
PubMed2003

Robust persistent neural activity in a model integrator with multiple hysteretic dendrites per neuron.

Short-term memory is often correlated with persistent changes in neuronal firing rates in response to transient inputs. We model the persistent maintenance of an analog eye position signal by an oculomotor neural integrator receiving transient eye movement commands. Previous models of this network rely on precisely tuned positive feedback with <1% tolerance to mistuning, or use neurons that exhibit large discontinuities in firing rate with small changes in eye position. We show analytically how using neurons with multiple bistable dendritic compartments can enhance the robustness of eye fixations to mistuning while reproducing the approximately linear and continuous relationship between neuronal firing rates and eye position, and the dependence of neuron pair firing rate relationships on the direction of the previous saccade. The response of the model to continuously varying inputs makes testable predictions for the performance of the vestibuloocular reflex. Our results suggest that dendritic bistability could stabilize the persistent neural activity observed in working memory systems.

Action Potentials↗
PubMed2003

History dependence of rate covariation between neurons during persistent activity in an oculomotor integrator.

Persistent firing in response to a brief stimulus is a neural correlate of short-term memory in a variety of systems. In the oculomotor neural integrator, persistent firing that encodes eye position is maintained in response to transient saccadic eye-velocity commands. To a first approximation, firing rates in the integrator vary linearly with eye position. Thus, viewed across many cells, the pattern of persistent firing in the integrator may be constrained to a unique line of stable states. Here this idea was tested by examining the relationship between firing rates of simultaneously recorded neurons. Paired recordings were obtained in awake goldfish from neurons in hindbrain area I, an essential part of the horizontal eye-position integrator. During spontaneous eye movements consisting of sequential fixations at different horizontal positions, the pair relationship between the majority of cells on the same side of the integrator was not unique: for a given rate of one cell, the rate of the paired cell assumed different values that depended systematically on the preceding saccade history. This finding suggests that the set of persistent firing states that encode eye position is not constrained to a unique line, and that models with stable states restricted to a such a line need to be modified accordingly.

Action Potentials↗
PubMed2002

Linear regression of eye velocity on eye position and head velocity suggests a common oculomotor neural integrator.

The oculomotor system produces eye-position signals during fixations and head movements by integrating velocity-coded saccadic and vestibular inputs. A previous analysis of nucleus prepositus hypoglossi (nph) lesions in monkeys found that the integration time constant for maintaining fixations decreased, while that for the vestibulo-ocular reflex (VOR) did not. On this basis, it was concluded that saccadic inputs are integrated by the nph, but that the vestibular inputs are integrated elsewhere. We re-analyze the data from which this conclusion was drawn by performing a linear regression of eye velocity on eye position and head velocity to derive the time constant and velocity bias of an imperfect oculomotor neural integrator. The velocity-position regression procedure reveals that the integration time constants for both VOR and saccades decrease in tandem with consecutive nph lesions, consistent with the hypothesis of a single common integrator. The previous evaluation of the integrator time constant relied upon fitting methods that are prone to error in the presence of velocity bias and saccades. The algorithm used to evaluate imperfect fixations in the dark did not account for the nonzero null position of the eyes associated with velocity bias. The phase-shift analysis used in evaluating the response to sinusoidal vestibular input neglects the effect of saccadic resets of eye position on intersaccadic eye velocity, resulting in gross underestimates of the imperfections in integration during VOR. The linear regression method presented here is valid for both fixation and low head velocity VOR data and is easy to implement.

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