Lashley concluded that memories had to be spread all over the brain, throughout all the tissue.
Why do strong emotions trigger the formation of strong?
Strong emotional experiences can trigger the release of neurotransmitters, as well as hormones, which strengthen memory, so that memory for an emotional event is usually stronger than memory for a non-emotional event.
What is Karl Lashley known for?
Equipotentiality is the theory that the brain has the capacity (in the case of injury) to transfer functional memory from the damaged portion of the brain to other undamaged portions of the brain.
Lashley pioneered experimental work conducted on rats with surgically induced brain lesions, by damaging or removing specific areas of a rat’s cortex, either before or after the animals were trained in mazes and visual discrimination.
Traditional view of Hebb in the current context
Hebb is best known for three primary contributions. First is the clear formalization of the notion of association through synaptic plasticity, now often referred to as the Hebbian synapse. Hebb himself never claimed that the idea was original. In fact, he was puzzled by the credit he received for the “fire together-wire together” idea (McNaughton, 2003), as it can be traced at least to Lorente de Nó (see above), and probably to James (1890) as well. Similar ideas can also be found in Alexander Bain’s 19th century book, Mind & Body, in which a simple network of neurons could support associative memory through distributed activity:
Moreover, as touched upon by P. Milner in correspondence with Orbach in 1996, the idea may even be traced back as far as the Greek philosophers (Orbach, 1998). Still, Donald Hebb has been credited with laying the theoretical framework leading to the discovery of “long-term potentiation” (LTP). One of the discoverers of LTP, Tim Bliss, was a graduate student at McGill in the early 1960s, working in the laboratory of the physiologist B.D. Burns. His dissertation work involved looking for sustained activity in slabs of neocortex – in essence a search for synaptic plasticity of the sort postulated by Hebb (Bliss et al., 1968; personal communication). Less than a decade later, Bliss found what he was looking for, and what Hebb had incorporated in his theory, not in neocortex, but in slices taken from the hippocampus (Bliss and Lomo, 1973).
Shying away from credit for the notion of synaptic plasticity, Hebb found his other theoretical postulates more interesting. Chief among them was the concept of the cell assembly. As noted, Hebb cited Lorente de Nó as the primary inspiration behind the concept of the cell assembly. As initially described by Hebb, cells with activity within a certain temporal window would undergo a shared growth if this activity is repeated. Energy propagation could be self-sustained through recurrent projections. The net effect of recurrent activation would be the development of a spatiotemporal pattern among the members of the assembly that would be readily re-activated should the initiating event occur again in the future. Hebb noted that the description was not fully developed: “This then is the cell-assembly. Some of its characteristics have been defined only by implication, and these are to be developed elsewhere, particularly in the remainder of the chapter (~4 pages), in the following chapter (“Ch. 5 Perception of a Complex: The Phase Sequence’), and in Chapter 8 (see pp. 195–197 ; reference to section titled “Metabolic Factors Disturbing Behavior’)” (italacize portions ours, Hebb, 1949).
Note that the way ‘cell assemblies’ are now discussed within neuroscience and psychology diverges in several ways from what Hebb proposed. Hebb’s assemblies were designed to capture temporal associations physiologically, by strengthening the link between neuron A and neuron B whenever activity in A is followed by activity in B. The focus was on sequence, but without dependence on sensory input, since the recurrent nature of the network would allow it to maintain its activity in the absence of such input. While Hebb’s definition made no mention of neurons of an assembly needing to be temporally synchronous, such synchronicity is assumed in more modern versions (Abeles, 2011). Moreover, Hebb’s original model was predicated solely on excitatory recurrent connections, as inhibitory synapses had not yet been firmly established. Both excitation and inhibition are part of current attempts to physiologically define cell assembly membership (Harris et al., 2003; Maurer et al., 2006). Indeed, we now know that such networks can even be comprised solely of inhibitory interneurons. The meaning of the term cell assembly is hence fluid and dependent upon its contextual use (Abeles, 2011).
Hebb also made a very important assumption about how a memory, in the guise of enhanced synaptic efficacy in a cell assembly, is formed in the brain. He suggested that the reverberation occurring within a cell assembly, initially triggered by some external input, can temporarily maintain the memory. Over time, these reverberations will initiate structural changes in the same set of synapses, and this will now constitute the permanent memory. The idea that short-term memory and long-term memory occur within the same circuits was discarded early on, as notions about systems-level memory consolidation emerged (e.g., Squire et al., 1984). We will return to this important thread in Hebb’s thinking below, as there is now considerable evidence that he was on the right track here.
Here, prior even to the neuron doctrine, Bain provided a connectionist idea of how the brain supports flexible behavior (Wilkes and Wade, 1997).
Hebb’s critical insight would seem to be his assertion that these recurrent neural networks were modifiable by experience. While others talked about synaptic plasticity and still others talked about recurrent networks, it was Hebb who saw the power of putting these two things together. Doing so lead to Hebb’s third major contribution: the idea that a trained neural network, complete with recurrent connectivity, would be capable of self-sustaining activity and effectively functioning as a closed system. While this concept of a “phase sequence” is often attributed to Hebb’s 1949 book, the etiology of the idea can be found in earlier works:
Interestingly, Hebb referenced Frank Beach and his investigations of the organization of courtship and copulation in the male, noting that many actions appear to be innately organized in the rat while, in the primate, there is an interaction between what is modified by experience and what is inherited. Through this, Beach concluded that “the circuits for organization of the motor acts may be subject to facilitative impulses from higher brain centers” (Beach, 1942). As Beach was also a student of Lashley, along with Hebb, it seems likely that they all shared discussions of how behavior seems to be both organized and adaptive – the major theoretical advance the “phase sequence” provides.
Hebb noted how the architecture set forth by Lorente de Nó could establish either stable, reinforcing dynamic patterns, or – perhaps challenged by fluctuation – result in an unstable, unpredictable pattern. Finally, Hebb stated in this early manuscript that learning would increase “cerebral organization” and hence more effectively organize behavior. Current understanding of the notion of a phase sequence invokes the concept of an assembly that assumes simultaneity of cellular activity (“fire together, wire together”), linking each assembly together in a chain through associative plasticity. By this conventional understanding, chains of cell assemblies equal a phase sequence. This formulation probably falls short of capturing what Hebb had in mind because it fails to properly emphasize two concepts: 1) reentrant loops provide a mechanism for self-sustaining activity and 2) cell assemblies can propagate activity through alternate anatomical pathways in a way that distributes the “engram”. This latter point is particularly crucial, as it allowed Hebb to argue that memory is indeed not localized in specific synapses, but in the trained neural network pathways through which activity moves.
It is worth noting that, based on his pedagogical training from Lashley, Hebb would most likely reject the contemporary definition of the phase sequence as it evokes descriptions of sequence chains and chaining. Following on from behaviorism, “chaining” is the idea that complex behavior is constructed through a series of smaller sequence-response events. Once learned, a stimulus can evoke a cascade of responses. Its shortcomings, as described by Terrance (“Intelligent behavior is greater than the sum of discrete conditioned responses” (2005)), echoed back to Karl Lashley, in his comprehensive attempt to capture the failings of the chaining theory which was most-likely prevalent in Lashley’s thoughts when working with Hebb; Lashley published his ideas in 1951. In describing complex movement, Lashley states:
Lashley drew evidence from a patient who most-likely suffered a spinal cord transection (dorsal column likely) but remained capable of moving his leg. The patient’s ability to initiate precise movements in the absence of proprioception showed that sensation is not necessary for appropriate responses. Second, Lashley noted that hand motions, such as that of a skilled pianist, occur faster than proprioceptive elements can be relayed back to the brain. Music at the arpeggio pace was far too fast to achieve sight reading or register the feedback sensation of the last moment to cue the next. A pianist, fingering at the rate of 16 key strokes per second, has coordinated movement that outpaces the reaction time of the visual system (Lashley 1951). Based on this evidence, Lashley rationalized that the brain must “chunk” information, taking in large blocks of written chords and translating them into a sequence of events to be executed with a predetermined intensity and duration. Lashley’s third objection to pure stimulus-response mechanisms, was that errors in motor or speech were often related to a higher cognitive process, involving anticipation or over correction. Lashley related his own typing experience — a typo in which he accidently omitted a letter resulted in an overcompensation shortly thereafter, adding one too many of the ‘lost’ letter somewhere else. From this, Lashley deduced that thought and motor execution must be independent. Further, he suggested that “conflicting impulses may distort the order”, which we interpret as Lashley suggesting that higher cognition can influence lower dynamics.
Lashley had a fourth reason to dismiss any form of connectionism – his own research on the impact of brain lesions, and of disconnecting various regions, on behavior, and in particular on perception, learning, and memory. These are the primary data that led Lashley to his talk about mass action and equipotentiality, for which he has been derided and ultimately ignored. But this is a mistake. Though some believe Equipotentiality and Mass Action to be theories put forward by Lashley, they “…were not the explanation he sought, but rather summary statements of observations which themselves needed explanation” (Hebb, 1959, p. 149). It is the data that need explaining, and this is not the place to do that job. Suffice it to say here that the methods in use at the time (lesions, etc) were not specific enough in their effects to support the conclusions that Lashley drew from them. Newer techniques have made it possible to track down particular “memories” to specific brain regions, even as they have shown that for the kind of memories of greatest interest to humans – our life’s events – it takes a network to get it done. But that is a topic for another time.
All these reasons put together led Lashley to dismiss sequence chaining as a mechanism of higher-cognition. He moved irrevocably away from the concept of a stable “engram” carried by a fixed series of connected neurons firing in a specific order. Hebb, too, was well aware of the shortcomings of the sequence chain hypothesis and noted that his own theory “is evidently a form of connectionism, one of the switchboard variety, though it does not deal in direct connections between afferent and efferent pathways: not an ‘S-R’ psychology, if R means muscular response”. This conclusion almost inevitably shares a common etiology with Lashley.
The mention by Hebb that his theory was a form of connectionism may seem strange to the modern reader. This likely shows the direct influence of Lashley on Hebb. More to the point, this caveat echoes a statement that came years prior:
Therefore, Hebb’s use of hedge words in his theory, “…evidently a form of connectionism…”, may signal genuflection towards Lashley (Boden, 2006), and it is important to reiterate that Hebb did not portray his theories as an absolute rejection of field theory. This deference from Hebb to Lashley necessitates serious consideration of the question posed by Glickman, “[What was the degree to which]…Lashley’s questions.set the agenda for Hebb’s answers…?” (Glickman, 1996). From the above quote, it can be inferred that Lashley required more evidence in support of the idea that local synaptic plasticity was the basis of memory (Orbach, 1998). The resurrection of synaptic plasticity as a memory mechanism can be readily credited to Hebb, whether he wanted the credit or not. To address Lashley’s concerns, Hebb offered his concept of the cell assembly, which used local synaptic plasticity to achieve some of the functions Lashley thought only a field theory could address. Importantly, both Hebb and Lashley built on the recurrent framework, drawn from the anatomical drawings of Lorente de Nó, as their starting platform. This framework has a traceable connection from Lashley to Hebb, even if indirect (Orbach, 1998). Lashley appreciated this anatomical architecture in 1938. Moreover, he sought an ‘in-person’ connection to Lorente de Nó notably during the time in which Hebb and Lashley were working together at Yerkes and three years prior to the publication of Hebb’s book ( ). Nevertheless, it was Hebb’s ingenuity that connected recurrent anatomy to synaptic plasticity as the physiological basis by which spatiotemporal patterns could be formed.
Therefore, while it appears that Lashley believed Hebb was misrepresenting the original ideas (see Rosenzweig’s account above), it seems more reasonable to argue that Hebb provided the logical extension of Lashley’s ideas (Glickman, 1996). In terms of similarity, Lashley favored the use of the word “trace” which shared a great deal with Hebb’s cell assembly:
Neurons, organized into the recurrent networks of Lorente de Nó, would generate a broad pattern of activity when excited, propagating like a wave (Lashley, 1942). This concept was later expanded on with parallels to Hebb’s phase sequence. Certain traces, supporting different functions such as memory or knowledge, can become active via external input and sustain their activity through recurrent projections. Moreover, one “trace” can activate another and “partial traces” can exist (Lashley, 1951; 1958).
The differences between the approaches are that Lashley (1) denied the relevance of specific synaptic connections and pathways, (2) strongly emphasized dynamics and (3) pushed a broader mechanism of reduplication through reverberation:
Thus, although there were similarities between Lashley and Hebb, this stands as clear evidence that theoretical differences could be identified as early as one year after the publication of Hebb’s book, and quite likely existed beforehand. Hebb’s inspiring framework, even in the absence of rigorous derivation (cf. MILNER, 1957) drove the field of neuropsychology forward. Noting that the initial definition of cell assembly was limited in terms of its description and drawing parallels between the assembly and a precious situation in a fission reactor, Milner introduced inhibition to the model (1957). He also added the use of simultaneous firing to identify neurons as part of a cell assembly, binding these cells into a group, and distinguishing them from those neurons that are not firing (Milner, 1957). Hebb took note and modified his own theory in 1982 to include inhibitory interneurons:
Perhaps in light of his views on mass action, Lashley may have argued that, although correlates exist, there are no special cells devoted to specific encoding tasks, say of faces, time or space. For example, with respect to hippocampal place cells, it is likely that Lashley would have argued that time and space are correlates inherent to a dynamic system:
Lashley viewed the perception of space and time as interchangeable (Nadine Weidman, personal communication) and thought that the act of moving activity across the brain is what is necessary for higher-cognition and memory. Both Hebb and Lashley felt that the system effectively creates its own time in that, similar to a pendulum, activity that returns via recurrent pathways to a particular population can define time with each volley of activity. While humans often consider time and space as independent entities, individual cells might have little to do with the encoding of these parameters. Rather, Lashley reasoned that reentrant processing – input spreading through recurrent connections in a series of repeating volleys – was the foundation of the brain as a dynamic system. Operationalizing this in terms of a mechanism that could support higher-cognition, Lashley weakly ventured that:
Lashley mulled this theory for many years with a description published as early as 1942:
This theoretical position was highlighted in the University of Rochester lecture in which Lashley described his research using low resistance conductors placed over the visual cortex in an attempt to distort the perceived visual input, along with experiments by Sperry, who implanted mica (an insulating medium) into the cortex. If the electrical field were important, this manipulation should “short” the potential between regions, presumably with negative consequences.
Perhaps these results led Lashley to refine his position. In an unpublished, undated manuscript, Lashley suggested that the wave analogy is illusory yet extended it to biological observations:
Distilled to its core, Lashley felt that interacting, reentrant loops of the nervous system generated patterns of neural firing that provided the basis for perception, cognition and action. Nonetheless, as the perpetual critic, Lashley conceded that his formulations and attempts to address these issues were not fully developed, applying to his own theory the same criticisms he levelled at Hebb. For his part, Hebb pointed out the limitations of the reverberatory mechanisms that Lashley was describing:
Moreover, Lashley’s implementation of analogy runs counter to his stance on the use of ‘farfetched’ equivalences as noted above. It is of interest to note that the analogy Lashley chose is neither digital nor man-made, but reflective of analog dynamics seen elsewhere in nature.
In addition to his promulgation of the notions of mass action and equipotentiality, Lashley is also known for his failed ‘search for the engram’. Lashley, however, did not believe he failed to find the engram as a consequence of lesioning the wrong brain region, but instead because the ‘engram’ itself might be a good deal more abstract than what had been thought, a very modern idea:
It is now commonplace to note that brains have evolved in order to adapt and predict in the service of survival and reproduction (for recent examples, see Buzsaki, 2006; Buzsaki, 2013). The simplest mechanism to achieve prediction, as seen in lower organisms, is a single stimulus-response loop. Higher order animals have multiple, layered loops with connections that allow complex network interactions. Patterns of activity through these networks are self-organized, long-lasting and adaptive.
For various reasons, some of the most impactful aspects of Lashley’s and Hebb’s work have been largely ignored. First, self-sustaining, reverberatory activity through reentrant processes is what defines “cell assemblies”, which serve as the building blocks of phase sequences, which in turn subserve complex behavior and higher cognition. While there is an allure to having a population code by which multiple neurons associate through plasticity, causing them to fire simultaneously, this was not part of Hebb’s original definition. Neither Hebb nor Lashley intended to describe a mechanism of how memories are stored – they were focused, as noted at the outset, on the more general issues of how neural mechanisms support coordinated behavior and the fundamental problems of “stimulus and response equivalence”. Second is the idea that activity in one loop, connected via synapses, can induce patterned activity in other loops. As Hebb invokes this, the patterned activity in other regions would effectively be anticipatory or predictive of what was about to occur in the environment following learning. One could say that this constitutes memory, and can be equated to modern ideas about pattern completion. Lashley, however, avoided ideas that placed emphasis on single cells or synapses. Rather, he saw the recurrent flow of activity as akin to waves and would most likely have taken a more dynamical perspective. Similar to Rayleigh–Bénard convection, Lashley’s approach suggests “pattern formation”, by which activity takes similar paths through recurrent networks, but in a manner significantly more malleable than the index theories that currently hold sway amongst hippocampal aficionados (Teyler and DiScenna, 1986). Recall that Lashley viewed the nervous system and its activity in terms of “statistical accuracy” (Lashley, 1957).
Third, as noted above, current theories of learning and memory invoke Hebbian synapses, diverging yet again from the original Hebbian concept. Hebb, like Lashley, diminished the importance of individual synapses:
Though there is an attraction to the causal nature of “fire together, wire together” by which associations are encoded in synapses, both Lashley and Hebb were reluctant to suggest that cause-and-effect are easy to uncouple in the nervous system. Rather, their perspective suggests that neuroscience should seek to uncover the rules that govern how the nervous system is predisposed to respond to inputs.
Finally, it is worth noting that Lashley was explicitly addressing a central question at the crux of the NIH BRAIN initiative: “Today we know that neurons fire and we know that they are connected. We don’t know how they act in concert to govern behavior, the essential question in treating neurological disease and mental-health disorders” (Allen and Collins, 2013). Lashley’s comments seem prophetic and anticipatory:
FAQ
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