Donald O. Hebb and the Organization of Behavior: 17 years in the writing

Abstract

The Organization of Behavior has played a significant part in the development of behavioural neuroscience for the last 70 years. This book introduced the concepts of the "Hebb synapse", the "Hebbian cell assembly" and the "Phase sequence". The most frequently cited of these is the Hebb synapse, but the cell assembly may be Hebb's most important contribution. Even after 70 years, Hebb's theory is still relevant because it is a general framework for relating behavior to synaptic organization through the development of neural networks. The Organization of Behavior was Hebb's 40th publication. His first published papers in 1937 were on the innate organization of the visual system and he first used the phrase "the organization of behavior" in 1938. However, Hebb wrote a number of unpublished papers between 1932 and 1945 in which he developed the ideas published in The Organization of Behavior. Thus, the concept of the neural organization of behavior was central to Hebb's thinking from the beginning of his academic career. But his thinking about the organization of behavior in 1949 was different from what it was between 1932 and 1937. This paper examines Hebb's early ideas on the neural basis of behavior and attempts to trace the rather arduous series of steps through which he developed these ideas into the book that was published as The Organization of Behavior. Using the 1946 typescript and Hebb's correspondence we can see a number of changes made in the book before it was published. Finally, a number of issues arising from the book, and the importance of the book today are discussed.

The Continuity of Context: A Role for the Hippocampus

“…Should the input change, so does the amorphous network. The dynamics of how the amorphous network changes in relation to input is most-likely non-linear (see Figure 3 Hebb's seminal cell assembly notion was inspired by what appeared to be recurrent neural networks captured by Lorente de No in his anatomical drawings of the hippocampal CA3 region (62)(63)(64). In these networks, Hebb imagined, "…excitation might theoretically continue for an indefinite period, 'chasing its tail', and not leave the circuit until some other excitation came along with which it might combine to produce a motor effect that neither could produce alone" (65, p. 56).…”

The Hebb Synapse Before Hebb: Theories of Synaptic Function in Learning and Memory Before Hebb (1949), With a Discussion of the Long-Lost Synaptic Theory of William McDougall

“…Synaptic function is not only essential for learning and memory ( Lisman et al, 2018 ) but synaptic dysfunction underlies both neurodevelopmental and neurodegenerative disorders of cognitive function ( Taoufik et al, 2018 ; Batool et al, 2019 ). For a further discussion of the relationship between the engram and Hebb’s theory see Brown (2020) .…”

“…He was compiling other people’s thoughts and postulates, and editing them so they could all work together as one clear explanation as to the physiological basis of learning. As noted by Hebb (1949 , p. 70), “The general idea is an old one, that any two cells or systems of cells that are repeatedly active at the same time will tend to become ‘associated’ so that activity in one facilitates activity in the other.” Earlier papers have discussed how Hebb developed the theory that was presented in 1949 (see Brown and Milner, 2003 ; Brown, 2017 , 2020 ) and this manuscript examines some of the theories that pre-dated Hebb’s synaptic theory. In researching this manuscript, we discovered the synapse theory of William McDougall, which seems to have been ignored by his contemporaries, so we summarize it here, as an example of an idea before its time (see Gross, 2009 ).…”

“…On the other hand, in his history of psychology Flugel (1933/1964 , p. 228) states that McDougall’s synaptic theory of consciousness, including his theory of inhibition by drainage was “the most successful neurological theory that has ever been proposed”; an opinion echoed by Cyril Burt (1939 , 1955) , a former student of McDougall. As discussed by Brown (2020) , Hebb had no concept of inhibition in his cell assembly hypothesis, although he did consider the problem of inhibition in early drafts of his theory. Hebb (1980 , p. 101) said that “the existence of a neural inhibition was not definitely known in 1949 and was not incorporated in the theory though it would have helped.…”

“…As discussed by Brown (2020) , there were a number of other synaptic theories of learning and memory in the early 1940’s which were outlined by Hilgard and Marquis (1940 , pp . 326–335 ) and Morgan (1943 , pp.…”