Search bioRxiv⌕ Search

Biology subjects

Frost, W. N.

Publications and source records attributed to Frost, W. N..

5 recordsLinked to original sources

A Self-Priming Neural Chain Links Sequential Behaviors Across Timescales

Behavioral sequences are essential for survival, yet the neural mechanisms that link one action to the next remain incompletely understood. In classical chain models, sequential behaviors arise through feedforward propagation of activity across distinct neuronal populations or network modules. Here, we identify a distinct form of neural chain mechanism in which neurons active during a first behavior modulate themselves into a persistent state of elevated tonic firing that subsequently drives the second behavior from within the first circuit module. We term this process self-priming, reflecting the role of activity-dependent auto-modulation in enabling behavioral sequencing. We investigated this mechanism in the escape swim-crawl sequence of the marine mollusk Tritonia diomedea, in which rhythmic swimming is consistently followed by tens of minutes of rapid crawling. Serotonergic dorsal swim interneurons (DSIs), components of the swim central pattern generator, were previously known to exhibit elevated firing for tens of minutes after a swim motor program (SMP) and to drive crawling. We show here that their sustained post-SMP activity arises from self-induced increases in DSI excitability: their bursting during the SMP produces long-lasting depolarization and enhanced excitability within the DSI population. This persistent state drives prolonged elevated tonic firing which, in turn, drives escape crawling. Our findings demonstrate a self-priming neural chain mechanism in which activity during one behavior generates the internal drive for the next. Unlike previously described feedforward chain mechanisms, sequencing in this system does not depend on sequential recruitment of distinct neural substrates. Instead, the same neurons participate continuously across both behaviors while their activity-dependent change in state links the two actions into a coordinated sequence. This mechanism provides an elegant and generalizable solution for linking sequential actions across timescales.

neuroscience↗

Age-related degradation of behavioral and network features of Aplysia escape locomotion

Aplysia californica has been a useful model system for studies of the neural basis of behavior, learning, and aging. While the latter topic has been explored with respect to several of its simple reflex behaviors, this study represents the first examination of how one of Aplysias more complex behaviors, escape locomotion, is affected in animals nearing the end of their natural lifespan. Old animals (12-13mo) showed a greatly reduced gallop response compared with middle-aged adults (5-7mo), together with a loss of locomotion onset latency sensitization. Large-scale VSD imaging was used to record motor programs in isolated brain preparations from middle-aged vs. elderly animals. Old brains displayed the same loss of onset latency sensitization seen in the intact old animal behavior, and also a reduced number of cycles per locomotion episode. Brains from middle-aged animals showed an unchanged number of motor program cycles from that observed in intact animals, but a much more transient motor program onset latency sensitization. A further age-related finding was that while in middle-aged brains repeatedly eliciting the motor program led to progressively increasing cumulative activity across trials, in old brains this same procedure led to progressively decreasing activity. Some of our results are consistent with peripheral processes working in concert with the CNS as animals age to support healthy locomotion behavior and its modification by learning, or with early changes in the brain that are not yet expressed in behavior.

neuroscience↗

Strategies used by two memories to share space in a common neural network

How distinct memories are encoded into the same network space without destructive interference is not well-understood. Here, we utilized Tritonia diomedeas escape swim network to explore how two sequentially acquired forms of non-associative learning, sensitization and habituation, are encoded into the same network. Behavioral experiments showed them to alter non-identical sets of behavioral features, suggesting they utilize somewhat independent sites of plasticity within the network. Large-scale voltage-sensitive dye recordings revealed two findings. First, both forms of learning, which occur sequentially in the 10-trial training protocol used, act to produce a change in the number of pedal neurons firing during the dorsal phase of the motor program, with sensitization producing an increase, and habituation a decrease in their number. The number of neurons participating in the ventral phase was unaffected. Second, sensitization produced an enhancement of burst intensity specific to the ventral phase neurons, while habituation was associated with a decrease in burst intensity in both phases. Using injected current pulses, intracellular recordings revealed that sensitization acted to increase the excitability of neurons firing in both phases, whereas habituation only acted to reduce excitability in ventral phase neurons. These excitability changes were associated with different mechanisms - reduced spike frequency accommodation in the ventral phase neurons, and depolarization of the resting potential in the dorsal phase neurons. These findings of partially different storage sites and mechanisms for two different non-associative memories illuminate a potential network strategy for minimizing destructive interference when storing multiple memories into the same network.

neuroscience↗

Neural division of labor: the gastropod Berghia defends against attack using its PNS to retaliate and its CNS to erect a defensive screen

Relatively little is known about how the peripheral nervous system (PNS) contributes to the patterning of behavior, in which its role transcends the simple execution of central motor commands or mediation of reflexes. We sought to draw inferences to this end in the aeolid nudibranch Berghia stephanieae, which generates a rapid, dramatic defense behavior, "bristling." This behavior involves the coordinated movement of cerata, dozens of venomous appendages emerging from the animals mantle. Our investigations revealed that bristling constitutes a stereotyped but non-reflexive two-stage behavior: an initial adduction of proximate cerata to sting the offending stimulus (Stage 1), followed by a coordinated radial extension of remaining cerata to create a pincushion-like defensive screen around the animal (Stage 2). In decerebrated specimens, Stage 1 bristling was preserved, while Stage 2 bristling was replaced by slower, uncoordinated, and ultimately maladaptive ceratal movements. We conclude from these observations that 1) the PNS and central nervous system (CNS) mediate Stages 1 and 2 of bristling, respectively; 2) the behavior propagates through the body utilizing both peripheral- and central-origin nerve networks that support different signaling kinetics; and 3) the former network inhibits the latter in the body region being stimulated. These findings extend our understanding of the PNSs computational capacity and provide insight into a neuroethological scheme that may generalize across cephalized animals, in which the CNS and PNS both independently and interactively pattern different aspects of non-reflexive behavior.

neuroscience↗

A spiral attractor network drives locomotion in Aplysia

The joint activity of neural populations is high dimensional and complex. One strategy for reaching a tractable understanding of circuit function is to seek the simplest dynamical system that can account for the population activity. By imaging Aplysias pedal ganglion during fictive locomotion, here we show that its population-wide activity arises from a low-dimensional spiral attractor. Evoking locomotion moved the population into a low-dimensional, periodic, decaying orbit -a spiral -in which it behaved as a true attractor, converging to the same orbit when evoked, and returning to that orbit after transient perturbation. We found the same attractor in every preparation, and could predict motor output directly from its orbit, yet individual neurons participation changed across consecutive locomotion bouts. From these results, we propose that only the low-dimensional dynamics for movement control, and not the high-dimensional population activity, are consistent within and between nervous systems.

neuroscience↗