Differences in Mnemonic Processing by Neurons in the Human Hippocampus and Parahippocampal Regions

Abstract

Different structures within the medial-temporal lobe likely make distinct contributions to declarative memory. In particular, several current psychological and computational models of memory predict that the hippocampus and parahippocampal regions play different roles in the formation and retrieval of declarative memories [e.g., Norman, K. A., & O'Reilly, R. C. Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning systems approach. Psychological Review, 110, 611-646, 2003]. Here, we examined the neuronal firing patterns in these two regions during recognition memory. Recording directly from neurons in humans, we find that cells in both regions respond to novel stimuli with an increase in firing (excitation). However, already on the second presentation of a stimulus, neurons in these regions show very different firing patterns. In the parahippocampal region there is dramatic decrease in the number of cells responding to the stimuli, whereas in the hippocampus there is recruitment of a large subset of neurons showing inhibitory (decrease from baseline firing) responses. These results suggest that inhibition is a mechanism used by cells in the human hippocampus to support sparse coding in mnemonic processing. The findings also provide further evidence for the division of labor in the medial-temporal lobe with respect to declarative memory processes.

Multiple repetitions reveal functionally and anatomically distinct patterns of hippocampal activity during continuous recognition memory

“…Consistent with previous findings from continuous recognition tasks (Brozinsky et al, 2005;Viskontas et al, 2006), hippocampal old/new effects took the form of relative reductions in activity for old compared to new items. In a significant extension to those previous findings, Johnson et al …”

“…To determine whether the two different response profiles seemingly evident within right hippocampus and left parahippocampal cortex were statistically dissociable, the parameter estimates from clusters uniquely exhibiting the different profiles within each region were submitted to ANOVAs [factors of repetition, material, and profile (categorical/graded)]. For both regions, ANOVA gave rise to a significant repetition × profile interaction [right hippocampus: F(2.8, 41.9) = 5.66, p < .005; left parahippocampal cortex: F(2.6, 39.2) = 6.46, p < .005].Consistent with previous findings from continuous recognition tasks (Brozinsky et al, 2005;Viskontas et al, 2006), hippocampal old/new effects took the form of relative reductions in activity for old compared to new items. In a significant extension to those previous findings, Johnson et al …”

“…Using fMRI, Brozinsky et al (2005) reported greater hippocampal activity for new items compared to old items that were repeated after short (2 or 8 intervening items) but not longer (16 or 32) inter-item lags. Analogous findings were reported in a human single-neuron recording study of continuous recognition: Relative to the baseline firing rate, most of the hippocampal cells responsive to new test items showed enhanced firing, whereas cells responsive to old items largely showed a reduction in firing rate (Viskontas et al, 2006;see Rutishauser et al, 2006, for similar recognition-related reductions in hippocampal single-neuron activity). Together, these findings suggest that, in the context of continuous recognition tasks in which the lag between first and second presentations is relatively short, old items are associated with a net reduction in hippocampal neural activity relative to the level of activity elicited by new items.…”

“…Enhanced hippocampal activity for new relative to old items has also been observed in studies employing continuous recognition memory tests (where old/new status of items is manipulated within a single list; e.g., Brozinsky et al, 2005;Viskontas et al, 2006). Using fMRI, Brozinsky et al (2005) reported greater hippocampal activity for new items compared to old items that were repeated after short (2 or 8 intervening items) but not longer (16 or 32) inter-item lags.…”

“…Such findings have been interpreted as evidence that the hippocampus is sensitive to stimulus novelty, with elevated activity reflecting an allocation of processing resources toward the encoding of novel items (e.g., Duzel et al, 2003;Stark & Okado, 2003; also see Stern et al, 1996). To further complicate matters, activity in the same hippocampal region can seemingly demonstrate enhancement to both recollected and new test items relative to items that are merely familiar, suggesting that recollection and encoding may be subserved by common or closely adjacent neuronal populations (Woodruff et al, 2005;Yonelinas et al, 2005).Enhanced hippocampal activity for new relative to old items has also been observed in studies employing continuous recognition memory tests (where old/new status of items is manipulated within a single list; e.g., Brozinsky et al, 2005;Viskontas et al, 2006). Using fMRI, Brozinsky et al (2005) reported greater hippocampal activity for new items compared to old items that were repeated after short (2 or 8 intervening items) but not longer (16 or 32) inter-item lags.…”