Time and treason to the trisynaptic teachings: Theoretical comment on Kesner et al. (2005).

Abstract

Early descriptions of the hippocampal formation emphasized the serial nature of its circuitry, a description that suggests even a focal lesion would break a chain of processing and leave the entire region inoperative. Nevertheless, R. P. Kesner, M. R. Hunsaker, and P. E. Gilbert (2005) show that rats with CA1 lesions, but not rats with CA3 lesions, were impaired on a task in which animals were required to make associations between an object and an odor that were separated by a brief (10-s) delay. The present commentary makes 2 points relevant to their findings. First, several lines of evidence suggest that CA1 can operate somewhat independently of CA3 in some instances. Second, it is unclear whether the delay interval acted directly (by requiring a memory for a timeline of events) or indirectly (by outlasting the associative abilities of areas other than CA1) in causing performance to depend on the integrity of CA1.

Comparative Cognition, Hippocampal Function, and Recollection

“…In contrast, rats with selective CA1 lesions showed no sign of acquiring the associations between temporally separated objects, whereas rats with CA3 lesions acquired the task just as rapidly as normal animals. These results, and other similar findings (Kesner et al, 2005), are consistent with the possibility that CA3 is specialized for the representation of items in the (spatial) context in which they are experienced, whereas CA1 is specialized for representation of the order of events that are separated in time (Manns & Eichenbaum, 2005). tive memory.…”

“…The resulting ROC analysis plots "hits," that is, correct identifications of old items, against "false alarms," incorrect identifications of new items as if they were old, across a range of confidence levels. This analysis typically reveals an asymmetric function characterized by an above-zero threshold of recognition at the most conservative criterion (zero false alarm rate) and thereafter a curvilinear performance function (Yofollowing considerations are based on recent and more extensive reviews covering each of these issues (Eichenbaum, 2004;Eichenbaum, Fortin, Ergorul, Wright, & Agster, 2005;Manns & Eichenbaum, 2005Eichenbaum, Yonelinas, & Ranganath, 2006), combined here to address the question of whether recollection is a cognitive function that is conserved across mammalian species.…”

Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 map

“…The data also suggest that the association with a spatial map is fundamental in CA3 and that its use of sparsely distributed firing fields can result in the binding of arbitrary information to space, in very much the same way as suggested by O'Keefe and Nadel (1978) for a cognitive map. The absence of recurrent connections downstream from CA3 seems to allow for the addition of information (e.g., nonspatial associations, sequence, time) Manns and Eichenbaum 2005;Rolls and Kesner 2006) for which the spatial map is not sufficiently versatile although the underlying spatial structure may remain partially preserved and can probably be recovered in the output returning to the parahippocampal cortices. Although the question remains why a system that performs several essentially nonspatial functions would need to be tied by such a large extent to place representations, the finding that the CA3 area efficiently preserves the spatial matrix to which arbitrary items can be attached rapidly (Leutgeb et al 2006b;Rolls and Kesner 2006;McHugh et al 2007) may be part of the answer.…”

Arc length coding by interference of theta frequency oscillations may underlie context-dependent hippocampal unit data and episodic memory function

“…Rats with full hippocampal lesions show impairments in retrieval on the basis of the temporal order of items (Fortin et al 2002;Kesner et al 2002), and selective CA1 lesions appear to cause greater impairments than CA3 lesions for memory of the temporal order of items (Lee et al 2005b;Rolls and Kesner 2006;Hoge and Kesner 2007). Region CA1 lesions but not CA3 lesions impair the ability of rats to perform a task in which an odor must be compared with the same or different odor after a 10-sec delay, suggesting a role for CA1 in Cold Spring Harbor Laboratory Press on April 7, 2019 -Published by learnmem.cshlp.org Downloaded from context-dependent timing of intervals (Kesner et al 2005;Manns and Eichenbaum 2005). Lower-frequency oscillations in more ventral entorhinal neurons could be important for timing of longer temporal intervals, as suggested by greater impairments of trace fear conditioning by ventral hippocampal lesions (Rogers et al 2006;Yoon and Otto 2007).…”