Spontaneous behaviors and evoked responses are traditionally viewed as separate and distinctly different phenomena. This distinction underlies the standard dichotomies between reflex and voluntary behaviors, and between evoked responses and the behavioral states or contexts in which they occur. In the typical tightly controlled laboratory environment, it is convenient to focus on stimulus-evoked behaviors and to treat spontaneous behaviors as simply nuisances to be minimized or averaged out. This focus ignores the critical role of spontaneous activity in creating the behaviors evoked by specific stimuli.
Drs. Wolpaw and Brembs will discuss recent vertebrate and invertebrate research indicating that spontaneous and evoked behaviors are not only inextricably linked but are, in important respects, no longer distinguishable from each other. This erosion of the traditional distinction is driven by the recognition that spontaneous variability is a necessary feature of all adaptive behaviors, and that even the simplest reflexes and stereotypic responses are controlled by sensory feedback. In contrast to the standard stimulus-response concept, the central thesis is that spontaneous behaviors provide a substrate that interacts with the environment so as to produce and maintain adaptive (i.e., appropriate) behaviors.
Dr. Wolpaw will discuss evidence that the quintessential evoked behaviors of vertebrates – reflexes mediated by spinal pathways – are highly plastic and display dependencies on past experience like those of spontaneous behaviors. The stimuli that evoke these reflexes are basically probes that assess ongoing spontaneous activity, and the resultant sensory feedback modifies that activity. Furthermore, the high variability of these reflexes underlies their adaptive capacities. He will also consider how the artificial behaviors created by brain-computer interfaces (BCIs) – behaviors produced by brain signals rather than muscles – arise largely from the interaction of spontaneous brain activity with sensory feedback. By connecting spontaneous activity to external consequences, BCIs create another situation in which spontaneous activity is shaped into adaptive behavior.
Dr. Brembs will discuss studies in several invertebrate species indicating that evoked behaviors are derived traits with reduced features, and have evolved from initially spontaneous behaviors. For example, in the fruit fly Drosophila, mathematical analyses of the temporal structure of spontaneous behavioral variability and genetic dissection of several feedback-based learning systems indicate that behavioral variability is not noise, but rather is essential to the brain’s capacity to use sensory feedback to create and maintain effective forward models for behavioral control. This function is implemented by a hierarchical interaction of learning systems (partially mediated by the mushroom-bodies) that shapes spontaneous actions into habitual responses.
In sum, converging evidence from disparate taxa and seemingly unrelated preparations indicates that spontaneous behaviors and evoked responses are opposite ends of the same spectrum. The data suggest that behavioral flexibility arises from an interaction of spontaneous and evoked behaviors that reflects individual history and genetic endowment and is continuously updated. This interaction maintains a balance between flexible exploration and efficient exploitation and ensures adaptive behavioral choice.