Uncovering temporal structure in hippocampal output patterns

Place cell activity of hippocampal pyramidal cells has been described as the cognitive substrate of spatial memory. Replay is observed during hippocampal sharp-wave-ripple-associated population burst events (PBEs) and is critical for consolidation and recall-guided behaviors. PBE activity has historically been analyzed as a phenomenon subordinate to the place code. Here, we use hidden Markov models to study PBEs observed in rats during exploration of both linear mazes and open fields. We demonstrate that estimated models are consistent with a spatial map of the environment, and can even decode animals’ positions during behavior. Moreover, we demonstrate the model can be used to identify hippocampal replay without recourse to the place code, using only PBE model congruence. These results suggest that downstream regions may rely on PBEs to provide a substrate for memory. Additionally, by forming models independent of animal behavior, we lay the groundwork for studies of non-spatial memory.

Inhibitory Units: An Organizing Nidus for Feature-Selective Sub-Networks in Area V1

SUMMARYSensory stimuli are encoded by the joint firing of neuronal groups composed of pyramidal cells and interneurons, rather than single isolated neurons (Uhlhaas et al, 2009, Buzsaki, 2010). However, the principles by which these groups are organized to encode information remain poorly understood. A leading hypothesis is that similarly tuned pyramidal cells that preferentially connect to each other may form multi-cellular encoding units yoked to a similar purpose. The existence of such groups would be reflected on the profile of spontaneous events observed in neocortical networks. We used 2-photon calcium imaging to study spontaneous population-burst events in layer 2/3 of mouse area V1 during postnatal maturation (postnatal day 8–52). Throughout the period examined both size and duration of spontaneously occurring population-bursts formed scale-free distributions obeying a power law. The same was true for the degree of “functional connectivity,” a measure of pairwise synchrony across cells. These observations are consistent with a hierarchical small-world-net architecture, characterized by groups of cells with high local connectivity (“small worlds”, cliques) connected to each other via a restricted number of “hub” cells” (Bonifazi et al., 2009, Sporns, 2011, Luce & Perry, 1949). To identify candidate “small world” groups we searched for cells whose calcium events had a consistent temporal relationship to events recorded from local inhibitory interneurons. This was guided by the intuition that groups of neurons whose synchronous firing represents a “temporally coherent computational unit” (or feature) ought to be inhibited together. This strategy allowed us to identify clusters of pyramidal neurons whose firing is temporally “linked” to one or more local interneurons. These “small-world” clusters did not remain static, during postnatal development: both cluster size and overlap with other clusters decreased over time as pyramidal neurons became progressively more selective, “linking” to fewer neighboring interneurons. Notably, pyramidal neurons in a cluster show higher tuning function similarity than expected with each other and with their “linked” interneurons. Our findings suggest that spontaneous population events in the visual cortex are shaped by “small-world” networks of pyramidal neurons that share functional properties and work in concert with one or more local interneurons. We argue that such groups represent a fundamental neocortical unit of computation at the population level.

Uncovering temporal structure in hippocampal output patterns

The place cell activity of hippocampal pyramidal cells has been described as the cognitive map substrate of spatial memory. Replay is observed during hippocampal sharp-wave ripple-associated population burst events and is critical for consolidation and recall-guided behaviors. To present, population burst event (PBE) activity has been analyzed as a phenomenon subordinate to the place code. Here, we use hidden Markov models to study PBEs observed during exploration of both linear mazes and open fields. We demonstrate that estimated models are consistent with temporal replay sequences and that the latent states correspond to a spatial map of the environment. Moreover, we demonstrate the identification of hippocampal replay without recourse to the place code, using only PBE model congruence. These results suggest that downstream regions may rely on PBEs to form a substrate for memory. Additionally, by forming models independent of animal behavior, we lay the groundwork for studies of non-spatial memory.

Head-Free Gaze Shifts Provide Further Insights Into the Role of the Medial Cerebellum in the Control of Primate Saccadic Eye Movements

This study examines how signals generated in the oculomotor cerebellum could be involved in the control of gaze shifts, which rapidly redirect the eyes from one object to another. Neurons in the caudal fastigial nucleus (cFN), the output of the oculomotor cerebellum, discharged when monkeys made horizontal head-unrestrained gaze shifts, composed of an eye saccade and a head movement. Eighty-seven percent of our neurons discharged a burst of spikes for both ipsiversive and contraversive gaze shifts. In both directions, burst end was much better timed with gaze end than was burst start with gaze start, was well correlated with eye end, and was poorly correlated with head end or the time of peak head velocity. Moreover, bursts accompanied all head-unrestrained gaze shifts whether the head moved or not. Therefore we conclude that the cFN is not part of the pathway that controls head movement. For contraversive gaze shifts, the early part of the burst was correlated with gaze acceleration. Thereafter, the burst of the neuronal population continued throughout the prolonged deceleration of large gaze shifts. For a majority of neurons, gaze duration was correlated with burst duration; for some, gaze amplitude was less well correlated with the number of spikes. Therefore we suggest that the population burst provides an acceleration boost for high acceleration (smaller) contraversive gaze shifts and helps maintain the drive required to extend the deceleration of large contraversive gaze shifts. In contrast, the ipsiversive population burst, which is less well correlated with gaze metrics but whose peak rate occurs before gaze end, seems responsible primarily for terminating the gaze shift.

Signal Propagation Along Unidimensional Neuronal Networks

Dissociated neurons were cultured on lines of various lengths covered with adhesive material to obtain an experimental model system of linear signal transmission. The neuronal connectivity in the linear culture is characterized, and it is demonstrated that local spiking activity is relayed by synaptic transmission along the line of neurons to develop into a large-scale population burst. Formally, this can be treated as a one-dimensional information channel. Directional propagation of both spontaneous and stimulated bursts along the line, imaged with the calcium indicator Fluo-4, revealed the existence of two different propagation velocities. Initially, a small number of neighboring neurons fire, leading to a slow, small and presumably asynchronous wave of activity. The signal then spontaneously develops to encompass much larger and further populations, and is characterized by fast propagation of high-amplitude activity, which is presumed to be synchronous. These results are well described by an existing theoretical framework for propagation based on an integrate-and-fire model.