Hill Of Activity Research Articles

Angular Path Integration by Moving “Hill of Activity”: A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System

During spatial navigation, the head orientation of an animal is encoded internally by neural persistent activity in the head-direction (HD) system. In computational models, such a bell-shaped "hill of activity" is commonly assumed to be generated by recurrent excitation in a continuous attractor network. Recent experimental evidence, however, indicates that HD signal in rodents originates in a reciprocal loop between the lateral mammillary nucleus (LMN) and the dorsal tegmental nucleus (DTN), which is characterized by a paucity of local excitatory axonal collaterals. Moreover, when the animal turns its head to a new direction, the heading information is updated by a time integration of angular head velocity (AHV) signals; the underlying mechanism remains unresolved. To investigate these issues, we built and investigated an LMN-DTN network model that consists of three populations of noisy and spiking neurons coupled by biophysically realistic synapses. We found that a combination of uniform external excitation and recurrent cross-inhibition can give rise to direction-selective persistent activity. The model reproduces the experimentally observed three types of HD tuning curves differentially modulated by AHV and anticipatory firing activity in LMN HD cells. Time integration is assessed by using constant or sinusoidal angular velocity stimuli, as well as naturalistic AHV inputs (from rodent recordings). Furthermore, the internal representation of head direction is shown to be calibrated or reset by strong external cues. We identify microcircuit properties that determine the ability of our model network to subserve time integration function.

Evidence against a moving hill in the superior colliculus during saccadic eye movements in the monkey.

Saccadic eye movements of different sizes and directions are represented in an orderly topographic map across the intermediate and deep layers of the superior colliculus (SC), where large saccades are encoded caudally and small saccades rostrally. Based on experiments in the cat, it has been suggested that saccades are initiated by a hill of activity at the caudal site appropriate for a particular saccade. As the saccade evolves and the remaining distance to the target, the motor error, decreases, the hill moves rostrally across successive SC sites responsible for saccades of increasingly smaller amplitudes. When the hill reaches the "fixation zone" in the rostral SC, the saccade is terminated. A moving hill of activity has also been posited for the monkey, in which it is supposed to be transported via so-called build-up neurons (BUNs), which have a prelude of activity that culminates in a burst for saccades. However, several studies using a variety of approaches have yet to provide conclusive evidence for or against a moving hill. The moving hill scenario predicts that during a large saccade the burst of a BUN in the rostral SC will be delayed until the motor error remaining in the evolving saccade is equal to the saccadic amplitude for which that BUN discharges best, i.e., its optimal amplitude. Therefore a plot of the burst lead preceding the "optimal" motor error against the time of occurrence of the optimal motor error should have a slope of zero. A slope of -1 indicates no moving hill. For our 20 BUNs, we used three measures of burst timing: the leads to the onset, peak, and center of the burst. The average slopes of these relations were -1.09, -0.79, and -0.58, respectively. For individual BUNs, the slopes of all three relations always differed significantly from zero. Although the peak and center leads fall between -1 and 0, a hill of activity moving rostrally at a rate indicated by either of these slopes would arrive at the fixation zone much too late to terminate the saccade at the appropriate time. Calculating our same three timing measures from averaged data leads us to the same conclusion. Thus our data do not support the moving hill model. However, we argue in the DISCUSSION that the constant lead of the burst onset relative to saccade onset (approximately 27 ms) suggests that the BUNs may help to trigger the saccade.

Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades.

1. In the companion paper we described two classes of cells in the monkey superior colliculus (SC) that were related to saccade generation, buildup cells and burst cells, which fell into two functional sublayers within the intermediate layers of the SC. Fixation cells in the rostral SC were deemed to be part of the buildup cell layer. The buildup cells had several characteristics in common with cells in the cat described as having a "hill of activity" moving across the SC, but the burst cells had no such characteristics. In this paper we further investigate whether there is evidence for such a moving hill of activity in the monkey by analyzing the spatial and temporal activity of cells across the SC during the generation of visually guided saccades. 2. We recorded the activity of single cells while the monkey made saccades of different amplitudes (0.5-60 degrees). We recorded cells from locations extending from the rostral to caudal SC in order to sample cells whose optimal amplitudes ranged from small to large saccades. This allowed us to see any shift of activity across the SC before, during, and after saccades. It also allowed us to determine the fraction of the SC that was active during the successive phases of saccade generation. 3. During active visual fixation, the fixation cells in the rostral pole of the buildup layer showed an increased discharge rate. From the population reconstruction, we estimate that the zone of active cells spanned the most rostral 0.72 mm in each SC. Assuming the SC is 5 mm in length, approximately 15% of the cells lying along the horizontal meridian in the buildup layer would be active during fixation. 4. At least 100 ms before the initiation of a saccade, long-lead activity began to appear in the buildup layer at the site on the SC motor map related to the next saccade. Fixation activity in the rostral poles simultaneously began to diminish, but the cells in the burst layer remained relatively silent. 5. Approximately 25 ms before saccade onset, the fixation cells ceased firing and both burst and buildup cells began to burst. The active zone in the burst layer was estimated to be approximately 1.4 mm diam, occupying roughly 28% of the SC along a line running from the rostral pole through the center of the initially active zone. The size of this active area among the burst cells was independent of saccade amplitude.(ABSTRACT TRUNCATED AT 400 WORDS)