Peter M. Milner (2000) Still in Search of the Engram?. Psycoloquy: 11(053) Autonomous Brain (5)

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PSYCOLOQUY (ISSN 1055-0143) is sponsored by the American Psychological Association (APA).
Psycoloquy 11(053): Still in Search of the Engram?

Reply to Dickinson on Milner on Autonomous-Brain

Peter M. Milner
Psychology Department
McGill University
1205 Dr. Penfield Ave.
Montreal, QC.


Dickinson takes a pessimistic view of the research aimed at understanding the engram. I consider that most of the required exploratory research has already been done and that further progress is hindered by a reluctance to abandon outworn ideas and interpretations.


association of ideas, attention, behaviour model, intention, motivation, self, serial order
1. Dickinson (2000) appears to approve of my general approach to the role of the nervous system in behavior, but believes I do not go far enough to explain the role of learning in development. Perhaps this criticism was written before Dickinson had penetrated to the later chapters of the book (Milner 1999a,b), in which I discuss a number of basic learning situations from the point of view of the thesis that response plans, not sensory input, drive behavior.

2. The same concentration on the earlier chapters may also account for Dickinson's criticism of my use of "black boxes". In fact of the 19 figures only 3 (2 of which are different levels of the same figure) are boxes with non-physiological content. They are intended to smooth the transition between behavioral and neural mechanisms. Many of the other figures are simplified neural diagrams used to help clarify the text; they are accompanied by a warning that such diagrams should not be taken too seriously.

3. Although I think it is a bit of a quibble, I do sympathise to some extent with Dickinson's criticism of my use of the word "engram". Lashley (1950) originally used the word to describe the neural substrate of the behaviorist's "stimulus"; the internal representation of an object that was supposed to become associated with a "response". My engram also consists of neurons at the interface of the perceptual and response systems, but it consists of neurons that have acquired connections from response plans. I suppose I thought "engram" was a concise, well-worn (even if somewhat moth-eaten) word that was ripe for recycling, so I redefined it for my own purpose.

4. The message I most wanted to get across in The Autonomous Brain is that we don't need to continue the search for Lashley's engram any longer. For almost 100 years, studies of perception have been based on the assumption that categories are immanent in the stimulus and can be teased out by clever neural circuitry, brute force, or evolution. How this could be when many stimuli fall into multiple categories is difficult to fathom. The more sophisticated theorists recognized that sensory input must be filtered by attention to make classification by subsequent circuits more feasible, but the source of the attention is usually vague, and the basic idea that the stimulus contains all the information needed for classification has still not been seriously challenged.

5. The neural model that I propose -- in which the intention to attain a goal sensitizes the organism to stimuli that will enable the requisite actions to be carried out -- is quite complicated. Dickinson accepts the model up to the point at which a plan arouses the associated percept neurons of what I call an engram, but he apparently considers my further analysis inadequate. Much hinges on my postulates concerning the sensory pathways. It is firmly established that neural connections link the different levels of the visual system in both directions. In the neocortex, the neurons comprising the interface with the response planning neurons are those in the inferior temporal lobe whose activity has been recorded by many investigators (e.g. Fuster et al. 1985; Gross et al, 1969; Miyashita, 1993). They respond to specific sensory features wherever they appear in a large part of the visual field. I speculate that they receive sensory input via complex converging paths that originate in "line" cells in the visual cortex. Some of the simpler circuits of these paths -- those that analyse angles and line-length ratios -- are described in more detail in an earlier paper (Milner, 1974). Running in the opposite direction are the returning axons of the attention path. Where the ascending path converges, the return path diverges, sensitizing the ascending relays it passes along the way. Thus a stimulus matching a need receives facilitation at all levels and is so intensified that it may suppress other sensory input by lateral inhibition.

6. Usually a planned response cannot be executed without information concerning the location of associated stimuli. This information cannot be obtained directly from the "engram" neurons, which are by definition insensitive to the location of the source. It must be derived from neurons nearer to the sensory input which have not lost positional input through convergence. Many of these neurons, however, are stimulated by sensory input from other than the required object. Those that correspond to the required object can only be identified by the fact that they are receiving feedback from engram neurons fired by the response plan, which intensifies their activity in comparison to that of other objects in the visual field. In this way, the activity of these neurons is selected for transmission (via a separate dorsal path) to the motor system to guide the response. This does not involve tautology. The dorsal path does not recognize the object whose dimensions and coordinates it is conveying to guide the musculature, it accepts the choice made at the interface of the ventral visual path and the response plan. A primary function of the "engram" neurons is to channel intentional activity (usually considered autonomous) to selected peripheral sensory neurons so that responses are directed to the intended objects.

7. Paragraph 7 of Dickinson's review assembles a flock of one-line criticisms and cavils apparently related to the binding problem. The attentional feedback system may provide a partial answer to the problem of how, in spite of being processed in different brain areas, all of a percept's features appear integrated into a single object. According to the model presented in the book, the attentional facilitation intensifies the activity of all neurons participating in the perception of the object being attended to, thus linking them together and preventing intrusions from other objects. Dickinson states: "As with Milner's short foray into the animal learning literature (in which he misses that the operant animal hardly needs to adapt to tasks of increasing levels of difficulty) [I am afraid that I still miss this point, my knowledge of the animal learning literature being limited] a short discussion of the human clinical literature on the neural mechanisms of memory... tends to concentrate on deficit behaviors." It is true that a good deal of the chapter on memory dwells on memory deficits, though there is a whole section on "Spared memory in amnesic patients" which belies Dickinson's remark that I "ignore the wealth of information available as a result of determining what amnesic patients can still do." It is a pity that Dickinson does not enlarge upon his puzzling (to me) comment that such determinations "might better inform the binding problem."

9. Dickinson's pessimism and negativism persists to the bitter end. After questioning whether a variety of topics, some of which are dealt with in the book and some of which are not, are "the core issues that the enigmatic engrams are intended to explain?" he is reminded of Pribram's (1971) admission that his search for the engram, like Lashley's, had failed -- the implication being that my efforts are doomed to the same fate. I like to think instead that Lashley and Pribram's engram never existed, being based on the mistaken idea that the meaning of a stimulus resides in the stimulus itself, and not on the effects it is capable of producing on living organisms. We shall not have a long wait, as Dickinson fears, for the empirical discoveries upon which a new interpretation of the engram can be based; some of them are already cited in "The Autonomous Brain."


Dickinson, A. R. (2000) Still in search of the engram? PSYCOLOQUY 11(037) psyc.00.11.037.autonomous-brain.3.dickinson

Fuster, J. M., Bauer, R. H. & Jervey, J. P. 1985. Functional interactions between inferotemporal and prefrontal cortex in a cognitive task. Brain Research, 330, 299-307.

Gross, C .G., Bender, D. B. & Rocha-Miranda, C. E. 1969. Visual receptive fields of neurons in inferotemporal cortex of the monkey. Science, 166, 1303-1306.

Lashley, K. S. 1950. In search of the engram. Symposia of the Society for Experimental Biology, 4, 454-482.

Milner, P. M. 1974. A model for visual shape recognition. Psychological Review, 81, 521-535.

Milner, P.M. (1999a) The Autonomous Brain. Erlbaum, Mahwah NJ

Milner, P.M. (1999b) Precis of "The Autonomous Brain" PSYCOLOQUY 10(071) psyc.99.10.071.autonomous-brain.1.milner

Miyashita, Y. 1993. Inferior temporal cortex: Where visual perception meets memory. Annual Review of Neuroscience, 16, 245-263.

Pribram, K. H. 1971. Languages of the brain. Monterey, CA: Brooks/Cole. Pp. 1-432.

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