Sensory Feedback Reduces Individuality by Increasing Variability within Subjects

Abstract

Behavioral variability is ubiquitous [1-6], yet variability is more than just noise. Indeed, humans exploit their individual motor variability to improve tracing and reaching tasks [7]. What controls motor variability? Increasing the variability of sensory input, or applying force perturbations during a task, increases task variability [8, 9]. Sensory feedback may also increase task-irrelevant variability [9, 10]. In contrast, sensory feedback during locust flight or to multiple cortical areas just prior to task performance decreases variability during task-relevant motor behavior [11, 12]. Thus, how sensory feedback affects both task-relevant and task-irrelevant motor outputs must be understood. Furthermore, since motor control is studied in populations, the effects of sensory feedback on variability must also be understood within and across subjects. For example, during locomotion, each step may vary within and across individuals, even when behavior is normalized by step cycle duration [13]. Our previous work demonstrated that motor components that matter for effective behavior show less individuality [14]. Is sensory feedback the mechanism for reducing individuality? We analyzed durations and relative timings of motor pools within swallowing motor patterns in the presence and absence of sensory feedback and related these motor program components to behavior. Here, at the level of identified motor neurons, we show that sensory feedback to motor program components highly correlated with behavioral efficacy reduces variability across subjects but-surprisingly-increases variability within subjects. By controlling intrinsic, individual differences in motor neuronal activity, sensory feedback provides each subject access to a common solution space.

Figure 1

How sensory feedback could affect motor variability. Center square shows a schematic of variability across and within animals in the absence of sensory feedback. Surrounding squares show possible effects of sensory feedback. Within-animal variability may decrease (left) or increase (right) for most animals; similarly, across-animal variability may decrease (bottom) or increase (top) for most animals. Within each square, box-and-whisker plots for data from three subjects are shown. Bottom and top whiskers correspond to the smallest and largest values, respectively; bottom and top of box correspond to the first and third quartile, respectively; the line within each box is the median value.

Figure 2

On average, variability across animals decreases but within animals increases in the presence of sensory feedback for a behaviorally relevant motor neuron. A. Box-and-whisker plots for the normalized duration of grasper motor neuron (B8a/B8b) activity recorded in seven different intact, behaving animals during multiple swallows induced by seaweed strips (n = 7, 10, 23, 5, 18, 9 and 7 swallows, respectively). B. Box-and-whisker plots for the normalized grasper motor neuron duration recorded in seven cerebral and buccal ganglia, in which motor programs were induced by application of the long-lasting cholinergic agonist carbachol to the cerebral ganglion [17] (n = 9, 7, 10, 18, 23, 7 and 5 ingestive motor patterns, respectively). The variability within several isolated ganglia without sensory feedback (animals 8, 9, 10, and 14) is lower than that observed in intact animals. In some isolated ganglia, within-animal variability increases (animals 11 and 13). The black box-and-whisker plots to the right of panels A and B combine the data from animals in each group; the overall variability is clearly lower in vivo than in vitro.

Figure 3

In the presence of sensory feedback, behavioral impact is associated with decreased across-animal variability and increased within-animal variability, and thus decreased individuality. A. Sensory feedback in vivo can induce decreases in across-animal variability and increases in within-animal variability. Plot axes are analogous to those of Figure 1. Each point represents the change in within-animal and across-animal variability in a single motor program component (Figure S3A). The change in variability of the data in Figure 2 is highlighted by a small square in Figure 3A (see text for details). Each motor program component was evaluated for its behavioral impact (see text). Points are colored from black (low behavioral impact) to green (high behavioral impact; scale between panels A and B). Changes in within- and across-animal variability are strongly correlated. B. Components with high behavioral impact always show decreases in individuality (average AUC) when sensory feedback is present. In contrast, motor program components with low behavioral impact show both increases and decreases in individuality when sensory feedback is present. Data from Figure 2 are highlighted by a small square in Figure 3B (see text for details).