Monkey hippocampal neurons related to spatial and nonspatial functions

Abstract

1. Neural activity in the monkey hippocampal formation (HF) was analyzed during a spatial moving task in which the monkey was guided by auditory and visual cues and when stimuli were presented from various directions. The monkey could control a motorized, movable device (cab) and its route to a target location by pressing the proper one of five available bars in an appropriate sequence (spatial moving task). In any of several locations in the field, neural responses were evident in relation to the presentation of various objects or human movement in some relative direction (left, anterior, right) as a directional stimulus test. 2. Of 238 hippocampal neurons analyzed, 172 (72.3%, 238-66) responded in either the spatial moving task, or to the direction from which stimulation was presented, or to the location of the monkey in the field, or to some combination of these. 3. The activity of 79 (33.2%) neurons was higher when the monkey was in some specific location in the field during the spatial moving task, regardless of the approach route or other task parameters (place related neurons). 4. Responses to the task cues in the spatial moving task were evident in 110 (46.3%) neurons (task related neurons). Of these, 77 (32.4%) neurons were not place related. The remaining 33 (13.9%) neurons were both task related and place related. These neurons responded to task cues in only that part of the field in which place related responses occurred. The neural response to the task cues disappeared when the monkey moved out of the place response region. The place related and task related neural responses disappeared when the room light was switched off. Thus information from the environment outside of the cab contributed to the place related and task related responses. 5. Stimuli presented from certain specific directions induced responses, selectively, in 41 (17.2%) of the neurons (direction related neurons). The dependence of the preferred direction was described in one of three ways--egocentric, allocentric, or place-direction specific. Nineteen egocentric neurons responded to a stimulus only when it was presented from a certain direction relative to the orientation of the monkey, regardless of the location of the monkey. Eleven allocentric neurons responded to a stimulus only when it was presented at a particular position in the room, regardless of the location or orientation of the monkey.(ABSTRACT TRUNCATED AT 400 WORDS)

Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats

“…The place cell of the rodent HF is characterized by location-specific firing (O'Keefe and Conway, 1978;Eichenbaum et al, 1987;McHugh et al, 1996;Skaggs and McNaughton, 1998), and comparable HF neuron responses were also reported in monkeys (Ono et al, , 1993Nishijo et al, 1997;Matsumura et al, 1999). Place-cell activity is controlled by a salient cue or multiple spatial cues (e.g., O'Keefe and Conway, 1978;O'Keefe and Burgess, 1996), and remains stable over a long period Thompson and Best, 1990).…”

Grid cells and cortical representation

“…Place cells and grid cells were discovered in rats but similar cells have subsequently been reported in mice [13][14][15] , bats 16,17 , monkeys [18][19][20][21] , and humans 22,23 , although the bulk of work on entorhinal-hippocampal spatial representation is still performed in rodents. The strong correspondence in each species between entorhinal-hippocampal firing patterns and a measurable property of the external world -the location of the animal -makes the spatial representation circuit a powerful experimental model system for understanding neural computation at the highest levels of the association cortices, many synapses away from sensory receptors and motor outputs.…”

Grid cells in mice

“…Whether entorhinal neurons have similar functional properties in other species than the rat remains to be determined. In the hippocampus, 'place cells' have been described in humans (Ekstrom et al, 2003), monkeys (Ono et al, 1991(Ono et al, , 1993Matsumura et al, 1999;Ludvig et al, 2004), bats (Ulanovsky and Moss, 2007), and mice (McHugh et al, 1996;Rotenberg et al, 1996), although it has been proposed that in the monkey hippocampus, discharge is more determined by what the animal sees than where it is (Rolls and O'Mara, 1995;Rolls et al, 1997). Because place cells are likely to be derived from grid cells (O'Keefe and Burgess, 2005;Fuhs and Touretzky, 2006;McNaughton et al, 2006;Solstad et al, 2006;Fyhn et al, 2007), grid cells may exist in a similar range of species.…”