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, 19 (6), 2381-93

Spatial- And Task-Dependent Neuronal Responses During Real and Virtual Translocation in the Monkey Hippocampal Formation

Affiliations

Spatial- And Task-Dependent Neuronal Responses During Real and Virtual Translocation in the Monkey Hippocampal Formation

N Matsumura et al. J Neurosci.

Abstract

Neuropsychological data in humans demonstrated a pivotal role of the medial temporal lobe, including the hippocampal formation (HF) and the parahippocampal gyrus (PH), in allocentric (environment-centered) spatial learning and memory. In the present study, the functional significance of the monkey HF and PH neurons in allocentric spatial processing was analyzed during performance of the spatial tasks. In the tasks, the monkey either freely moved to one of four reward areas in the experimental field by driving a cab that the monkey rode (real translocation task) or freely moved a pointer to one of four reward areas on the monitor (virtual translocation task) by manipulating a joystick. Of 389 neurons recorded from the monkey HF and PH, 166 had place fields that displayed increased activity in a specific area in the experimental field and/or on the monitor (location-differential neurons). More HF and PH neurons responded in the real translocation task. These neurons had low mean spontaneous firing rates (0.96 spikes/sec), similar to those of rodent HF place cells. The remaining nonresponsive neurons had significantly higher mean firing rates (8. 39 spikes/sec), similar to interneurons or theta cells in the rodent HF. Furthermore, most location-differential neurons showed different responses in different tasks. These results suggest that the HF and PH are crucial in allocentric information processing and, moreover, that the HF can encode different reference frames that are context or task-dependent. This may be the neural basis of episodic memory.

Figures

Fig. 1.
Fig. 1.
Schema of the experimental setup and paradigm.A, Freely movable monkey cab (a) and front panel of the cab (b). A monkey sat in a 0.7 × 0.8 × 0.85 m cab, which was freely moved in a 2.5 × 2.5 m experimental field located in a 5.0 × 6.0 m room. The front wall of the cab was made of transparent Plexiglass, and the rear wall was a steel plate symmetrically equipped with two speakers on the inside. On the upper part of the front wall, there was a 10.4-inch color LCD monitor with resolution of 640 × 480 pixels. The visual stimuli were displayed 25 cm from the monkey’s eyes on the color LCD controlled by a microcomputer. The lower part of the front wall was equipped with a joystick to freely move a cab in the experimental field and/or a pointer (a yellow sphere with a radius of 3 mm) presented on the LCD monitor. The cab and/or the pointer could be moved at constant velocity (3 cm/sec in real space and 2.5 mm/sec in virtual space, respectively) in all directions during continuous manipulation of the joystick by the monkey. The movement direction of the cab and/or the pointer was linked to the direction to which the joystick was brought down by the monkey. Thick curved lines with arrows in Aa and Abindicate examples of movements of the cab and the pointer to one of destinations indicated by thick circles[TA in Aa]. Juice reward, controlled by an electromagnetic valve, was delivered from a tube that projected through the rear wall. B, Time sequence of the four behavioral tasks. The monkey performed the four behavioral tasks under guidance by visual stimuli on the LCD monitor and auditory stimuli from the two speakers on the back wall of the cab. The four tasks consisted of five phases: (1) pretrial control (the cab placed at a starting point); (2) warning period (a warning tone from the 2 speakers plus a window frame on the LCD monitor were presented for 1 sec); (3) discrimination phase (a red target circle with a radius of 1.59 cm appeared on the LCD monitor for 2 sec); (4) manipulating–response phase (the monkey manipulated the joystick); and (5) reward phase (a reward of ∼6 ml of orange juice for 3 sec was delivered).
Fig. 2.
Fig. 2.
Spatial arrangements of room cues and target areas for the RT task (A) and those of target circles on the LCD monitor for the RT and VT tasks (B). A, The monkey sat in a chair in a cab and could see various landmarks in the experimental room, such as a stereomicroscope, a refrigerator, a table, a rack, and some experimental devices, which were available to identify its position in the experimental field. In the RT tasks, the monkey moved the cab to one of four reward areas in the four corners of the experimental field (TA1–TA4) by manipulating the joystick. Area in the thick-lined box, 2.5 × 2.5 m experimental field; area in the dotted-lined box, range of movement of a center of the cab where the monkey sat in a chair.Refrig, Refrigerator; Stereotaxic, stereotaxic apparatus; Oscillo, oscilloscope;Expri, experimenter; D.W., microcomputer for Datawave; Amp, main amplifier; Contr, task controller; PC-98, microcomputer for monitoring movements of the cab and joystick. B, A window frame indicated by a thick-lined box, which was proportional to the experimental field at the ratio of 1:12.61, appeared on the LCD monitor with a warning tone. In the VT tasks, the monkey moved a pointer on the LCD monitor to one of four reward areas in the four corners of the LCD monitor (TC1–TC4) by manipulating the joystick. In the RT tasks, one of the four target circles, each of which corresponded to each of the target areas in the experimental field, was presented on the LCD monitor to specify the destination. Area in the dotted-lined box, Range of movement of the pointer on the LCD monitor.
Fig. 3.
Fig. 3.
Two typical examples of the HF neurons.A, An example of an HF neuron with location-differential responses. Aa, The trail of the cab (left panel) and the corresponding location-differential responses (right panel) in the RT/TC task. A place field is surrounded by thick lines. Calibration is shown at the right; a mean firing rate for each pixel was expressed as a relative firing rate in which the mean firing rate in each pixel was divided by the grand mean firing rate in each task and was shown in five steps (R ≥ 2M; 2.0M > R ≥ 1.5M; 1.5M > R ≥ 1.0M; 1.0M > R ≥ 0.5M; R < 0.5M). Three values in the calibration indicate those of 2M, M, and 0, respectively. Regions not visited by the monkey during the session(s) are shown by blank pixels. Note that the activity increased in the right back corner of the experimental field, although the monkey moved and visited various sites of the experimental field and received juice reward at the four corners of the experimental field. Ab, Superimposed spike waves of the HF neuron shown in Aa. Ac, Autocorrelogram of the HF neuron shown in Aa. Ordinate, Number of spikes; abscissa, time in msec; bin size, 1 msec. Note that a refractory period of the neuron was 2–3 msec, which indicated that these spikes were recorded from a single neuron.B, An example of an HF neuron without location-differential responses. Note that no place fields were observed. Other descriptions as in A.
Fig. 4.
Fig. 4.
Trails of a cab and firing rate maps of the HF location-differential neuron shown in Figure 3A during the successive three sessions in the RT/TC task. A–C, Individual trail and firing rate maps during the three sequential sessions in the RT/TC task. D, Average trail and firing rate maps during the three sequential sessions in the RT/TC task. Note that the place fields in these three sessions overlapped and were highly consistent. Other descriptions as in Figure 3.
Fig. 5.
Fig. 5.
Relationship between eye movements and activity of the neuron shown in Figures 3 and 4 during the RT/TC task.A–C, Independent activity of the neurons, regardless of eye movements. Eye trace, Left eye positions; Cab location, location indicated by coordinates inx- and y-axes; X, coordinates in x-axis; Y, coordinates iny-axis; Raster, raster display of neuronal activity. R, Right; L, left;U, up; D, down. Hatched bars, Duration of cab movements; light stippled areas, duration during which a cab was located within a place field of the neuron. D, Trials of a cab during the RT/TC task. Trails indicated by labels A, B, and C in D correspond to cab movements in panels A–C. Place fields of the neurons are shown by a light stippled area. Arrows, Directions of cab movements.
Fig. 6.
Fig. 6.
An example of trail and firing rate maps of the RT/TC-responsive HF neurons that had place fields only in the RT/TC tasks (Table 1, RT/TC only). Note that the neuron had two place fields at the left front corner of the experimental field in the RT/TC tasks (A). Other descriptions as in Figure 3.
Fig. 7.
Fig. 7.
An example of trail and firing rate maps of the RT/TC-responsive HF neurons that had place fields in the RT/TC, RT/P-TC, and VT/P tasks (Table 1, RT/TC + RT/P-TC + VT/P). Note that the HF neurons had partially overlapped place fields. In the RT/TC (Ab) and RT/P-TC (Bb) tasks, the place fields in the right back area of the experimental field overlapped, but place field was located around the right forward area on the window frame of the LCD monitor in the VT/P task (Cb). Other descriptions as in Figure 3.
Fig. 8.
Fig. 8.
An example of trail and firing rate maps of the RT/TC-responsive neurons that had place fields in the RT/TC, VT/P and VT/P-TC tasks (RT/TC + VT/P + VT/P-TC in Table 1). Note that the HF neurons had partially overlapped place fields. In the RT/TC and VT/P tasks, the place fields in the left front area on the frame overlapped (Ab, Cb), but the place field was located around the right downward area on the window frame in the VT/P-TC task (Db). Other descriptions as in Figure 3.
Fig. 9.
Fig. 9.
An example of trail and firing rate maps of the HF neurons that had place fields in the RT/P-TC but not in the RT/TC tasks (Table 1, RT/P-TC-responsive without responses to RT/TC). Note that the HF neurons had completely overlapped place fields. There were overlapped place fields around the center of the frame in the RT/P-TC (Bb) and VT/P-TC (Db) tasks. Other descriptions as in Figure 3.
Fig. 10.
Fig. 10.
An example of trail and firing rate maps of the HF neurons that had place fields only in the VT tasks (Table 1, Nonresponsive to RT). Note that the HF neuron had completely overlapped place fields in both the VT/P (Cb) and VT/P-TC (Db) tasks. Other descriptions as in Figure3.
Fig. 11.
Fig. 11.
An example of trail and firing rate maps of the HF neurons that had place fields in the RT/TC and VT/P-TC tasks (Table1, RT/TC + VT/P-TC). Note that the HF neuron had nonoverlapped place fields. The HF neuron had two place fields in the right forward corner of the experimental field in the RT/TC task (Ab), whereas it had a place field in the left lower corner of the LCD monitor in the VT/P-TC task (Db). Other descriptions as in Figure 3.
Fig. 12.
Fig. 12.
Locations and sizes of the place fields in the four different tasks. Aa–Ad, Locations and sizes of the HF and PH neurons that had place fields in the RT/TC (n = 119, Aa), RT/P-TC (n = 73, Ab), VT/P (n = 72, Ac), and VT/P-TC (n = 66, Ad) tasks. Note that place fields distributed randomly and covered most areas of the experimental field and the LCD monitor. B, Relative sizes of the place fields (see Materials and Methods for definition of the relative size of a place field). *p < 0.05; **p < 0.01, significant difference from the mean relative size of the place field in the VT/P-TC task by Newman–Keuls test after one-way ANOVA (F(3,326) = 5.654; p < 0.01).
Fig. 13.
Fig. 13.
Comparison of spontaneous firing rates among the four types of the HF and PH neurons. A, Distributions of spontaneous firing rates of the three types of location-differential and nonresponsive neurons in Table 1. Note that most location-differential neurons had low spontaneous firing rates of <5 spike/sec, whereas mean spontaneous firing rates of the nonresponsive neurons distributed widely from low to high spontaneous firing rates.B, Comparison of mean spontaneous firing rates of the four types of the HF neurons. *p < 0.01, significant difference from the mean spontaneous firing rate of the nonresponsive neurons by Newman–Keuls test after one-way ANOVA (F(3,385) = 17.789; p < 0.01).
Fig. 14.
Fig. 14.
Recording sites of various neuron types in monkey HF and PH. Numbers below each section indicate distance (in millimeters) from interaural line. Most of the HF neurons were recorded from the CA1 and CA3subfields, the dentate gyrus (DG), and thePH; some were recorded from the subiculum (SUB). Note that various types of location-differential neurons distributed widely in various areas of the HF and PH, and no significant segregation of specific types of neurons was observed.LV, Lateral ventricle.

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