Dissociable areas of memory (in MTL): Two or three?

There has been some discussion in memory literature as to whether familiarity / novelty detection and recollection (contextual recognition of a stimulus or episodic recall) are independent processes or are the same processes, but only the memory strength varies.

In 2006, an fMRI study came around that showed that there were three dissociable areas in MTL that were associated with familiarity, novelty and recollection detection.

There have been indications that recollection, familiarity, and novelty involve different medial temporal lobe subregions, but available evidence is scarce and inconclusive. Within the medial temporal lobes (MTLs), they found a triple dissociation among the posterior half of the hippocampus, which was associated with recollection, the posterior parahippocampal gyrus, which was associated with familiarity, and anterior half of the hippocampus and rhinal regions, which were associated with novelty. Furthermore, multiple regression analyses based on individual trial activity showed that all three memory signals, i.e., recollection, familiarity, and novelty, make significant and independent contributions to recognition memory performance.

This appeared to be the established dogma to me, till I came across this new PNAS paper, which again strives to swing the pendulum back in favor of memory strengths and a single process for recollection and familiarity/novelty detection. The authors found that while a distinct group of neurons in hippocampus and anygdala was responsible for novelty and familiarity detection, recollection could just be ascertained by the strength of the neural firing of these groups of neurons. Here is the abstract of the study:

Episodic memories allow us to remember not only that we have seen an item before but also where and when we have seen it (context). Sometimes, we can confidently report that we have seen something (familiarity) but cannot recollect where or when it was seen. Thus, the two components of episodic recall, familiarity and recollection, can be behaviorally dissociated. It is not clear, however, whether these two components of memory are represented separately by distinct brain structures or different populations of neurons in a single anatomical structure. Here, we report that the spiking activity of single neurons in the human hippocampus and amygdala [the medial temporal lobe (MTL)] contain information about both components of memory. We analyzed a class of neurons that changed its firing rate to the second presentation of a previously novel stimulus. We found that the neuronal activity evoked by the presentation of a familiar stimulus (during retrieval) distinguishes stimuli that will be successfully recollected from stimuli that will not be recollected. Importantly, the ability to predict whether a stimulus is familiar is not influenced by whether the stimulus will later be recollected. We thus conclude that human MTL neurons contain information about both components of memory. These data support a continuous strength of memory model of MTL function: the stronger the neuronal response, the better the memory.

PNAS has made the article freely available, so go have a look. This is what they discuss:

We analyzed the spiking activity of neurons in the human MTL during retrieval of declarative memories. We found that the neural activity differentiated between stimuli that were only recognized as familiar and stimuli for which (in addition) the spatial location could be recollected. Further, we found that the same neural activity was also present during behavioral errors, but with reduced amplitude. This data are compatible with a continuous signal of memory strength: the stronger the neuronal response, the better the memory. Forgotten stimuli have the weakest memory strength and stimuli that are only recognized but not recollected have medium strength. The strongest memory (and thus neuronal response) is associated with stimuli that are both recognized and recollected.

One methodological flaw of the current study is that it didn’t take the earlier studies showing triple dissociation into account and did not differentiate between MTL neurons based on their location within hippocampus/ amygdala. If they had distinguished based on the location, they might have found some neurons that were selectively coding for recollection. In absence of such observations I find it hard to concur that recollection is not an independent process from familiarity/ novelty detection. Recollection involves binding the familiarity/ novelty cues with other neuronal cues in MTL like neurons that code for time and place . It may be that the current study completely missed out on those integrator neurons.

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