WOLF SINGER'S COMMENTARY

Commentary by Wolf Singer on ‘Effector patterns of basic emotions’, by S.Bloch, P. Orthous and G. Santibáñez, J. Social Biol Structures, 1988. 11, 207-209

A neurobiological evaluation of Susana Bloch's approach inevitably leads to a discussion of brain organization. Central questions in this context are, how particular functional states of the brain are stabilized and how transitions between these states can be accomplished. These questions are intimately related to the problem of how decisions are reached in complex and distributed systems.
Classical concepts of the brain have emphasized its modularity and hierarchical organization. The conceptual framework of this approach emerged originally from reflex theory and later from stimulus response paradigms of behaviorism. The brain was considered as an interface between the sensory surfaces which provide the brain with relevant information from its environment and effector organs which mediate the responses of the brain to changes in the environment. The task of the brain was thought to consist of adjusting reactions to changes in the environment as a function of stored information about the success or failure of previous responses to disturbances.  Furthermore, it was an implicit assumption that the brain as a serial interface between sensory and effector organs is itself hierarchically structured, decisions for the programming of coordinated behavioral responses being taken by centers occupying the highest levels in brain hierarchy.

On the basis of this conceptual framework, one would predict that the chances of success of Susana Bloch's approach are minimal. It would seem rather unlikely that particular central states would be inducible by modifying output patterns.  One would rather predict that the appropriate way to induce specific changes in central states would involve selective modification of sensory stimuli.  The brain would then adjust its central state to altered input in a more or less deterministic way.

Since Susana Bloch's approach is obviously successful and demonstrates convincingly that central states of the brain can be modified through a selective modification of output patterns, her approach challenges the classical concept of a hierarchically organized and essentially stimulus-dominated brain.  This is a very timely issue because there is indeed now an overwhelming body of data on the structural and functional organization of the mammalian brain which supports the notion that the basic algorithms of brain functioning may indeed differ radically from the organization outlined above.  First, it has become clear that the brain does not depend on signals from its sense organs for activation.  The brain constantly generates highly organized patterns of activity which designate well defined functional states. This is seen most clearly during early development when brain structures are spontaneously active and when this activity is used to promote the development of the system. Correlated activity patterns are used during this phase to identify functionally related neuronal centres and to establish selective connections between them.  Another example from the mature system for ordered self-generated activity is sleep.  Here, also, the brain generates highly organized activation patterns in the absence of any meaningful sensory stimulation.  The vividly experienced dreams which are completely unrelated to any simultaneous sensory input are a particularly impressive support for this fact.  Second, the concept of a serial organization of the brain with high-level structures in the hierarchy reserved for the central co-ordination of brain states has not received any experimental support. It turns out that there is no such unifying, decision-making center in the brain which would occupy the top position in a pyramid of sub-ordinated centres and which could be made responsible for a centralized co-ordination of state transitions. Neuroanatomical and neurophysiological data rather favor the notion that the brain is a highly distributed system consisting of many specialized modules which are massively interconnected with each other through reciprocal connections and function in parallel. Even though we lack full understanding of how decisions are reached in such a distributed system and how the various modules are coordinated in order to yield functional unity, we are led to conclude that transitions between states are not the result of a central command emitted from an unidentified meta-structure but result from ‘democratic’ interactions between modules all acting at the same level of hierarchy.  Third, recent anatomical and electrophysiological data provide convincing evidence against the notion that the central nervous system functions as a serially organized stimulus-response machine in which the flow of information mainly unidirectional from receptor surfaces to processing units and subsequently to effector organs. Quite on the contrary, the main connectivity scheme seems to be one of reciprocity. With only a few exceptions, both sensory and effector organs are linked to the nervous system with reciprocal connections. Thus, the brain has the option of controlling the sensory inflow already at the most peripheral levels and very often these efferent connections are more numerous than the afferent sensory pathways.  Likewise, any adjustment of effector organs by efferent pathways is signaled back to a large number of brain centers by re-afferent feedback loops.  In addition to these peripheral feedback loops there are further numerous internal connections between motor and sensory centers which serve to inform sensory processing areas about self-generated activation states.
It follows as one obvious consequence from these new concepts on brain organization that the central state of the brain is not solely determined by the pattern of sensory input but is the result of a very large number of variables whereby self-generated activation patterns play at least as important a role as stimuli from outside.  In particular, it is not too difficult to imagine on the basis of such extensive reciprocity that repeated execution of particular responses can, through back-propagation, recruit activation patterns in brain centers which are not directly involved in the execution of responses but which through previous learning have been associated by selective stabilization of pathways with particular response patterns. Thus, if particular activation states in brain centers responsible for the coding of emotional contents have been associated previously through learning or through inborn connections with certain behavioral responses, it is not difficult to see how execution of the behavioral response can lead through reciprocal connections to the reactivation of the corresponding activation pattern in emotion-coding structures.  In this context, Susana Bloch's approach can actually be considered as a psychophysical experiment aimed at testing the working hypothesis that there is back-propagation from behavioral responses to motivational states.  The outcome of her experiments clearly argues against the classical way to consider the nervous system as a stimulus-response machine and is in excellent accordance with the more modern view that emphasizes parallelity and reciprocity as the main organizational principles of the brain.  These principles of organization imply that self-generated activation patterns and stimulus-independent fluctuations between different behavioral states are presumably much more important determinants for actual states than afferent sensory signals.

W. Singer
Max Planck Institute for Brain Research,
Deutschordenstrasse 46, 6000 Frankfurt 71, FRG