Characterizing Changes in Functional Connectivity that Underpin a Learned Feeding Behavior
Post by Cody Walters
What’s the science?
Learning a new behavior necessitates changes in patterns of synaptic connectivity. While studies often focus on how these changes occur at individual locations in the brain, multiple regions undergo synaptic modifications during memory formation. This week in The Journal of Neuroscience, Tam et al. characterize a suite of synaptic changes affecting several sensorimotor pathways following learning in Aplysia (sea slugs).
How did they do it?
The authors trained Aplysia (sea slugs) by presenting them with tough, inedible food (seaweed wrapped in a plastic net). Initially, food presentation triggered biting and swallowing behavior, but over the course of training the Aplysia learned to reject the food (i.e., expel it from their mouths without attempting to swallow it). Animals were tested the following day to ensure long-term memory formation. The authors then extracted the buccal ganglia for electrophysiological analysis. The buccal ganglia contain mechano-afferents (which receive sensory information from the mouth) as well as interneurons and motor neurons that synapse on buccal muscles. These muscles play a central role in a variety of feeding behaviors such as protraction and retraction of the radula, the Aplysia’s tongue-like structure. The authors then conducted current-clamp recordings in individual neurons in the buccal ganglia preparations using glass electrodes.
What did they find?
The authors found that trained Aplaysia rejected a non-food item (a cannula) more rapidly than the naive Aplysia, a finding which suggests that the memory formed during training with the inedible food translated to a more general bias toward rejection behavior. To investigate the neural correlates of this learned rejection bias, the authors examined the monosynaptic connection between sensory neurons (group S1 buccal ganglia mechano-afferents) and their downstream interneurons/motor neuron targets (called ‘followers’). They electrically stimulated S1 neurons with a depolarizing current and recorded from follower neurons involved in feeding behavior. They discovered a diverse connection profile, with a subset of followers receiving unique combinations of excitatory and inhibitory projections from S1 mechano-afferents.
In trained Aplysia relative to naive controls, they found 1) an increase in the excitatory strength of S1-to-B4/B5 connections (B4/B5 neurons coordinate food rejection motor patterns), 2) an increase in the inhibitory strength of S1-to-B3 connections (the B3 motor neuron innervates musculature that retracts the radula and thus draws food particles into the oral cavity), and 3) an increase in the excitatory strength of S1-to-B61/B62 connections (B61/B62 motor neurons innervate musculature that protracts the radula and thus expels of food particles from the oral cavity). Additionally, they observed alterations in the strength and sign of the connections between the mechano-afferents and their downstream targets. Further, the authors found that the patterns of connectivity consistent with a food rejection bias were still maintained in the presence of multiple S1 spikes (in addition to a single S1 spike). Altogether, these synaptic modifications are consistent with a behavioral bias toward food rejection.
What’s the impact?
Tam et al. explored the neural basis of a learned behavior in Aplysia: a bias to reject food. While on the surface this behavior may appear uncomplicated, the changes that have to occur at the synaptic level to orchestrate this learned response are complex. This study mapped out distinct sensorimotor circuits that undergo specific synaptic modifications following training with inedible food that are consistent with a learned rejection bias. This ability to interrogate a macroscopic behavior by dissecting synaptic alterations across a range of individual neurons is an exciting development in the field of functional connectomics.
Tam et al. Multiple local synaptic modifications at specific sensorimotor connections after learning are associated with behavioral adaptations that are components of a global response change. The Journal of Neuroscience (2020). Access the original scientific publication here.