Adaptation towards scale-free dynamics improves cortical stimulus discrimination at the cost of reduced detection.

Fundamental to the function of nervous systems is the ability to reorganize to cope with changing sensory input. Although well-studied in single neurons, how such adaptive versatility manifests in the collective population dynamics and function of cerebral cortex remains unknown. Here we measured population neural activity with microelectrode arrays in turtle visual cortex while visually stimulating the retina. First, we found that, following the onset of stimulation, adaptation tunes the collective population dynamics towards a special regime with scale-free spatiotemporal activity, after an initial large-scale transient response. Concurrently, we observed an adaptive tradeoff between two important aspects of population coding-sensory detection and discrimination. As adaptation tuned the cortex toward scale-free dynamics, stimulus discrimination was enhanced, while stimulus detection was reduced. Finally, we used a network-level computational model to show that short-term synaptic depression was sufficient to mechanistically explain our experimental results. In the model, scale-free dynamics emerge only when the model operates near a special regime called criticality. Together our model and experimental results suggest unanticipated functional benefits and costs of adaptation near criticality in visual cortex.

Cortical Entropy, Mutual Information and Scale-Free Dynamics in Waking Mice.

Some neural circuits operate with simple dynamics characterized by one or a few well-defined spatiotemporal scales (e.g. central pattern generators). In contrast, cortical neuronal networks often exhibit richer activity patterns in which all spatiotemporal scales are represented. Such "scale-free" cortical dynamics manifest as cascades of activity with cascade sizes that are distributed according to a power-law. Theory and in vitro experiments suggest that information transmission among cortical circuits is optimized by scale-free dynamics. In vivo tests of this hypothesis have been limited by experimental techniques with insufficient spatial coverage and resolution, i.e., restricted access to a wide range of scales. We overcame these limitations by using genetically encoded voltage imaging to track neural activity in layer 2/3 pyramidal cells across the cortex in mice. As mice recovered from anesthesia, we observed three changes: (a) cortical information capacity increased, (b) information transmission among cortical regions increased and (c) neural activity became scale-free. Our results demonstrate that both information capacity and information transmission are maximized in the awake state in cortical regions with scale-free network dynamics.

Millisecond, micron precision multi-whisker detector.

The neural mechanisms of somatosensory information processing in the rodent vibrissae system are a topic of intense debate and research. Certain hypotheses emphasize the importance of stick-slip whisker motion, high-frequency resonant vibrations, and/or the ability to decode complex textures. Other hypotheses focus on the importance of integrating information from multiple whiskers. Tests of the former require measurements of whisker motion that achieve high spatiotemporal accuracy without altering the mechanical properties of whiskers. Tests of the latter require the ability to monitor the motion of multiple whiskers simultaneously. Here we present a device that achieves both these requirements for two-dimensional whisker motion in the plane perpendicular to the whiskers. Moreover, the system we present is significantly less expensive (<$2.5 k) and simpler to build than alternative devices which achieve similar detection capabilities. Our system is based on two laser diodes and two linear cameras. It attains millisecond temporal precision and micron spatial resolution. We developed automated algorithms for processing the data collected by our device and benchmarked their performance against manual detection by human visual inspection. By this measure, our detection was successful with less than 10 µm deviation between the automated and manual detection, on average. Here, we demonstrate its utility in anesthetized rats by measuring the motion of multiple whiskers in response to an air puff.