Learning modifies the functional connectome at multiple sites via different synaptic mechanisms to generate an appropriate behavioral response

Background:

Learning may produce a range of coordinated behavioral changes. These could arise by modifying a single site, secondarily causing multiple downstream modifications, or by directly modifying many sites. Long-term memory in an experimentally advantageous mollusc Aplysia trained with inedible food is expressed by multiple behavioral changes. One change is an increased bias to reject food or non-food objects. Another is cessation of responses to a specific food. We examined neural mechanisms underlying the different changes in behavior

Results:

Increased rejection arises in part by directly modifying in different ways synaptic connections from primary mechanoafferents in the buccal ganglia to followers with different functions. In connections to different followers, modifications include: changing the probability that cells are connected; changing excitation to inhibition and vice versa; and changes in amplitude.

Cessation of responses and specificity of learning to a particular food arise in part by a reduction in response in the cerebral ganglion to ACh, the neurotransmitter released by chemosensory afferents sensing food on the lips.

Conclusion:

The functional connectome (the set of neurons active while performing a behavior) must be changed when behavior is changed. Our data show that the functional connectome is changed by learning at a variety of different sites, by a variety of cellular mechanisms. Access to presynaptic and postsynaptic neurons will allow the identification of the signals and the mechanisms producing the individual changes that together lead to a global change in behavior, and help clarify the logic of learning at the synaptic level.