Expectation: Is Stimulus-Specific Apparent Anticipation a Sign of Higher Function?

  • Theodore Holmes Bullock


The nervous system shows adaptation by preparedness in a variety of ways, passive and active, genetic and learned, both for normal, unimportant input and for normal, important input that is either temporally anticipated or expected without temporal specification. The modalities and submodalities of sense organs, their receptive fields, filter properties, distributions, and sensitivities constitute a first order set of genetically in-built adaptations for the broad range of biologically important stimuli the given species can expect. Lower and higher central circuits and an array of behaviors in each species, innate and learned, manifest readiness for normally expected food, predators, social partners and common environmental features with aids for stimulus acquisition, such as control of posture, probing, and sampling rate. Learned expectations include short term and long term memories.

Physiological specializations at intermediate levels of the brain are differentially developed among taxa as well as among modalities. Efferent control of sense organs, usually reducing responsivity, is well developed in some species, modalities or submodalities. Some receptors are controlled by autonomic efferents that enhance responsivity.

Compensatory reflexes are numerous and widespread; probably none is universal. Their distribution and correlation with habit of life remain important problems in comparative physiology. The same is true of central compensations such as “space-constant” visual units that shift receptive fields with head tilt. Some mechanisms can be regarded as subtracting expected input to improve the detection of novel signals. Others selectively enhance important input.

Central neurons of some variety fire in consequence of commands to effectors (“corollary discharge”) and exert various effects upon the evaluation of input, especially reafference. The effect is plastic in some cases, such as electroreception in mormyrids, adjusting to the prevailing reafference. Such corollary discharge is absent in another group of electric fish, the gymnotiforms, and is, therefore, an evolutionary option among the mechanisms for distinguishing novelty from background.

“Common mode” or “in-phase rejection” is apparently used in the first electrosensory relay nucleus by elasmobranchs to improve the detection of unanticipated signals in face of certain kinds of self-generated noise.

Spikes from single units and compound waves are often signs of apparently anticipated or of unanticipated input for which the system is prepared. Units include extrapolating cells, comparator cells, habituated and conditioned cells and cells responsive only to complex stimuli like those from natural, important sights and sounds. Waves of compound field potentials may follow important ethological events or missing stimuli, “oddball” or “mismatch” stimuli.

My answer to the title question is, Yes, but in number, variety and sophistication, not in the simple presence of apparent expectation, which is a general property of living systems. Opportunities for new research abound; I would emphasize the comparison of species,the search for “subtraction” effects between as well as within modalities and the search for complex recognition neurons (see Chapter 8, “Recognition”), known in a few cases (hands, faces, songs) to be matched to frequently important input.


Contingent Negative Variation Electric Organ Discharge Electric Fish Orienting Reflex Corollary Discharge 
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© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Theodore Holmes Bullock
    • 1
  1. 1.Department of Neurosciences 0201University of California, San DiegoLa JollaUSA

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