Hippocampal mechanisms for the context-dependent retrieval of episodes

Abstract

Behaviors ranging from delivering newspapers to waiting tables depend on remembering previous episodes to avoid incorrect repetition. Physiologically, this requires mechanisms for long-term storage and selective retrieval of episodes based on time of occurrence, despite variable intervals and similarity of events in a familiar environment. Here, this process has been modeled based on physiological properties of the hippocampal formation, including mechanisms for sustained activity in entorhinal cortex and theta rhythm oscillations in hippocampal subregions. The model simulates the context-sensitive firing properties of hippocampal neurons including trial specific firing during spatial alternation and trial by trial changes in theta phase precession on a linear track. This activity is used to guide behavior, and lesions of the hippocampal network impair memory-guided behavior. The model links data at the cellular level to behavior at the systems level, describing a physiologically plausible mechanism for the brain to recall a given episode which occurred at a specific place and time.Keywords entorhinal cortex; dentate gyrus; region CA3; region CA1; spatial alternation; single unit recording; theta phase precession; current source density A waiter only takes orders once from each customer at each mealtime in a restaurant. Similarly, a foraging rat should avoid immediate return to a food cache where it just ate all the food. The ability to avoid repeating a completed behavior in a highly familiar environment depends on the ability to selectively retrieve recent episodes based on temporal context (e.g. in order to remember which customers or garbage cans were visited in a given time period).The context-sensitive properties of the spiking activity in the hippocampus may provide physiological mechanisms for this process. Some hippocampal neurons ("splitter cells" or "episodic cells") fire selectively dependent on the context of a specific recent response or future goal (Wood et al., 2000;Frank et al., 2000;Ferbinteanu and Shapiro, 2003). For example, during performance of a spatial alternation task, many hippocampal pyramidal neurons fire selectively after right turn or left turn trials, even though the rat is running in the same direction through the same location on the stem of the maze on both types of trials, as shown in Figure 1 (Wood et al., 2000). The model presented here shows how this activity may depend upon selective retrieval of prior episodes of behavior.During recordings on a linear track, other neurons show systematic changes in phase relative to theta frequency (7 Hz) oscillations in the hippocampal EEG (O'Keefe and Recce, 1993; Address correspondence to: Prof. Michael E. Hasselmo, Department of Psychology Center for Memory and Brain, Boston University, 2 Cummington St., Boston, MA 02215, (617) 353−1397, FAX: (617) Skaggs et al., 1996;Huxter et al., 2003). However, this theta phase precession does not appear on the first trial of the day, but appears on later trials of each day (Mehta ...

Phase Precession Through Synaptic Facilitation

“…Another class of phase precession models explicitly requires a network of neurons. Some of these network models suggest the origin of phase precession to be in CA3 (Tsodyks et al, 1996;Wallenstein & Hasselmo, 1997;Bose & Recce, 2001;Booth & Bose, 2001;Scarpetta & Marinaro, 2005) and others in the entorhinal cortex (Yamaguchi, 2003;Hasselmo & Eichenbaum, 2005). Finally, Jensen and Lisman (1996), Hasselmo et al (2002), Koene et al (2003), and Lisman et al (2005) predict phase precession to be generated through an interplay of the entorhinal cortex and CA3.…”

“…The classical point of view is that the mossy fiber synapse acts as a detonator that reliably transfers dentate activity into the cornu ammonis (McNaughton & Morris, 1987;Urban, Henze, & Barrionuevo, 2001). This detonator property has been exploited in models using the mossy fiber connections as teacher input (Treves & Rolls, 1992) and to mediate context retrieval (Hasselmo & Eichenbaum, 2005).…”

“…Recently phase precession has been reported in layer II of the medial entorhinal cortex (Fyhn, Hafting, Moser, & Moser, 2006), which provides input to the hippocampus. The origin of phase precession is still unknown, despite elegant experiments that aimed at unraveling underlying mechanisms (Ekstrom, Meltzer, McNaughton, & Barnes, 2001;Huxter et al, 2003;Zugaro, Monconduit, & Buzsáki, 2005), and despite reasonable effort to put forth mechanistic models (O'Keefe & Recce, 1993;Tsodyks, Skaggs, Sejnowski, & McNaughton, 1996;Jensen & Lisman, 1996;Wallenstein & Hasselmo, 1997;Bose & Recce, 2001;Harris et al, 2002;Hasselmo, Canon, & Koene, 2002;Mehta et al, 2002;Koene, Gorchetchnikov, Cannon, & Hasslemo, 2003;Lengyel, Szatmary, & Erdi, 2003;Yamaguchi, 2003;Huhn, Orban, Erdi, & Lengyel, 2005;Scarpetta & Marinaro, 2005;Lisman, Talamini, & Raffone, 2005;Hasselmo & Eichenbaum, 2005).…”

Affective, Natural Interaction Using EEG: Sensors, Application and Future Directions

“…Delta waves (0-3.5 Hz) occur in deep sleep [9]. Theta waves (3.5-7.5 Hz) have been associated with drowsiness, daydreaming, creative inspiration and meditation, arousal [6], sensorimotor processing and mechanisms of learning and memory [10]. Alpha waves (7.5-12 Hz) are present during wakeful relaxation with closed eyes and are reduced with open eyes, drowsiness and sleep.…”

“…Alpha waves (7.5-12 Hz) are present during wakeful relaxation with closed eyes and are reduced with open eyes, drowsiness and sleep. Mu waves (8)(9)(10)(11)(12)(13) Hz) are diminished with movement or an intent to move, or when others are observed performing actions. Beta waves (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) are associated with focus, concentration, high alertness, agitation and anxiety.…”