The role of sensory network dynamics in generating a motor program

Abstract

Sensory input plays a major role in controlling motor responses during most behavioral tasks. The vestibular organs in the marine mollusk Clione, the statocysts, react to the external environment and continuously adjust the tail and wing motor neurons to keep the animal oriented vertically. However, we suggested previously that during hunting behavior, the intrinsic dynamics of the statocyst network produce a spatiotemporal pattern that may control the motor system independently of environmental cues. Once the response is triggered externally, the collective activation of the statocyst neurons produces a complex sequential signal. In the behavioral context of hunting, such network dynamics may be the main determinant of an intricate spatial behavior. Here, we show that (1) during fictive hunting, the population activity of the statocyst receptors is correlated positively with wing and tail motor output suggesting causality, (2) that fictive hunting can be evoked by electrical stimulation of the statocyst network, and (3) that removal of even a few individual statocyst receptors critically changes the fictive hunting motor pattern. These results indicate that the intrinsic dynamics of a sensory network, even without its normal cues, can organize a motor program vital for the survival of the animal.

Figure 1.

A typical motor response during an episode of fictive hunting. This episode is one of nine recorded in this trial. A, Extracellular recordings from tail and wing motor nerves. Above each trace are color bars indicating the time of different color-coded sorted units. B, An overlay plot of the different sorted units in the left tail nerve in A. In this panel, the sorting includes all the episodes in the trial. C, 3D plot of the clustering of the units in B. Each spike is plotted according to its first three PCs. The color scheme is in accordance with B. The number of spikes in each cluster is between 40 and 690.

Figure 2.

A-C, Firing distribution of selected units from the tail and a wing nerves during different episodes of hunting from three experiments. Spike numbers were counted in 500 ms bins, and the activity was aligned to the beginning of the episode. The bottom of each panel is the summarized distribution calculated by averaging the corresponding bins in all the episodes above. The labels on the top left corner of each panel indicate the nerve that the unit was recorded from. The numbers on the y-axis indicate the frequency scale. L, Left; R, right; Tl, tail.

Figure 3.

Firing pattern of SRC populations during hunting episodes. A-C, Three examples of SDFs recorded from the STN in different experiments. Each color represents an identified unit, the spikes of which were detected and translated into SDF (see Materials and Methods). Each experiment is different in terms of the recorded units and patterns. Although the activity of several units can overlap, the temporal activation shown in this figure is sequential in the sense that the peaks of unit activity are distributed over the duration of the hunting episode.

Figure 4.

Relationship between spatiotemporal patterns during hunting episodes; similar spatiotemporal activity in the STN corresponds to a similar pattern in the motor nerves. A, Examples of normalized SDFs from the STN during three episodes of fictive hunting. These recording were performed in the same animal, and five different SRC units were sorted. B, SDF from wing motor nerves during the corresponding hunting episodes. C, Three-dimensional representation of the responses in A using the first three PCs as axes (red, top panel in A; green, middle panel in A; blue, bottom panel in A). D, Three-dimensional representation of the responses in B using the first three PCs as axes (colors as in C).

Figure 5.

The correlation of distances between all STN episode patterns and motor episode patterns for all animals in which recording from the STN has been performed (arbitrary units). Lines are the linear fits of the corresponding experiment depicted in a different color. Only the experiment in black is not significantly correlated (p = 0.08).

Figure 6.

The motor response to a brief stimulation of the STN without addition of physostimine. A, Schematic diagram of the experimental setup. The STN is a small nerve coming out of the statocyst into the cerebral ganglion where the SRC network is formed. The figure schematically depicts the connection between two SRCs (red and green) of the left statocyst. STIM, Stimulation; REC, recording. B, Extracellular recording from wing and tail nerves after a brief stimulation of the STN (the arrow marks the end of the 500 ms stimulation). C, Firing rate of the different motor units from B. The long dynamics of the response is similar to the motor activity dynamics during fictive hunting. D, Simultaneous extracellular recordings of wing, tail, and statocyst nerves from a separate experiment. All nerves showed the prolonged activation of multiple units typical of fictive hunting. The time interval when the amplifier was switched to stimulation mode was removed from the recordings. The black bar indicates the exact time of stimulation.

Figure 7.

Firing distribution of units from the left and right tail nerves and a left wing nerve (Wn) during fictive hunting before and after ablation of three SRCs. The burst were aligned to the beginning of the hunting episode. Note the change in the type of activity in some of the units.

Figure 8.

The average first PC before (blue) and after (red) ablation of three SRCs. A, Wing; B, left tail nerve; C, right tail nerve. The shaded regions denote a range of ±1 SD from the mean (n = 7). Note regions without overlap in A and C, which are regions that substantially changed.

Figure 9.

Change in cross-correlation of the first PC from Figure 7 before and after ablation of three SRCs for all possible nerve pairs. This cross-correlation was normalized so that the auto-correlations at 0 lag were equal to 1.