Neuroscience Letters, 109 (1990) 293-298 293 Elsevier Scientific Publishers Ireland Ltd.

NSL 06658

Recognition of egocentric and allocentric visual and auditory space by neurons in the hippocampus of

monkeys

Ryoi Tamura , Taketoshi Ono, Masaji F u k u d a and Kiyomi N a k a m u r a

Department of'Physiology, Faculty of Medicine, Toyama Medical and Pharmaceutical University, Toyama (Japan)

(Received 28 August 1989; Revised version received 13 October 1989; Accepted 16 October 1989)

Key words: Spatial memory; Egocentricity; Allocentricity; Hippocampus; Monkey; Single-unit recording

Neuronal activity in the hippocampus was recorded in the awake monkey during presentation of visual and auditory stimuli from various directions. About 10% of the neurons coded visual and/or auditory in- formation from unique directions. Some of these neurons were stimulus-selective, and others were not. Three types of neurons were identified by rotating the animals: egocentric and allocentric, and indetermi- nate. The results are consistent with a role of the hippocampus in spatial memory.

It has been suggested that the hippocampus is important for spatial memory. Hu- mans with right temporal lobe damage exhibited spatial memory deficits [18]. In monkey and rodent, bilateral lesions of the hippocampus produced impairment in spatial memory tasks [3, 8, 12, 14, 22]. In rats, unit recording studies suggested the existence of'place units' in the hippocampus that responded preferentially to particu- lar locations of the animal in the field [9, 11]. In primates, unit recording studies also suggested that there are hippocampal neurons that differentially respond in a delayed spatial response task [2, 21], a conditional spatial response task [7], and object-place memory tasks [2, 17]. However, relations between responses of neurons involved in spatial memory and properties of the stimuli (sensory modalities, physical property of stimuli, etc.) or the animal's own position have not been determined. To inves- tigate these relations, we analyzed responses of hippocampal single neurons in the monkey to presentation of various visual and/or auditory stimuli from various direc- tions in a few of the animal's positions in the experimental room.

Two monkeys (Macacafuscata), weighing 4.5-5.3 kg, were used. The monkeys were restrained painlessly in a stereotaxic apparatus by a previously prepared, surgically

Correspondence: T. Ono, Department of Physiology, Faculty of Medicine, Toyama Medical and Pharma- ceutical University, Toyama 930-01, Japan.

0304-3940/90/$ 03.50 © 1990 Elsevier Scientific Publishers Ireland Ltd.

294

fixed head holder. They sat in a chair facing an apparatus that was used for operant tasks and presentation of objects from anterior direction. The range of monkey's vi- sion was restricted to about + 80 ° from center by attaching opaque acrylic plates to the sides of the monkey's face. In this situation, the monkeys were presented with various visual and/or auditory stimuli from various directions, and extracellular ac- tivity and electrooculograms were recorded, and neuronal responses were analyzed [10, 13]. Some visual stimuli were apples, raisin, spider model, stick, human actions, etc. Many different auditory stimuli were used. Examples were computer synthesized sounds (harmonic rich or pure tones), human voice, monkey cry, step, clap, crash, and others. When a stimulus was considered to contain visual and auditory compo- nents, we attempted to separate the modalities by attenuating the intensity of the sound or masking it with white noise, and by reducing illumination to a minimum or restricting the monkey's vision with opaque plates. Responses to a given stimulus were tested by rotating the monkey and changing spatial relations between the mon- key and actual or potential environmental cues to determine the influence of these maneuvers on the responsiveness of the neuron.

Of neurons tested in the hippocampus and adjacent areas 86/837 (directional re- sponsive/tested) (dentate gyrus, 22/189; CA3 subfield, 23/162; CAI subfield, 28/299; subicular complex, 10/85; entorhinal cortex, 2/38; parahippocampal cortices, 1/64) responded (all by excitation) preferentially to some direction of visual and/or audi- tory stimuli. Activity of some of the directional neurons was complex. The sponta- neous firing rates of the directional neurons were low (2.95+2.92 spikes/s, mean + S.D., n = 86). The responses of the directional neurons did not correlate with particular movements of the monkey, such as eye or hand movement. Of 86 neurons tested, 44 responded only to visual stimuli (9 left anterior, 2 anterior, 30 right anter- ior, 3 multidirectional), 30 only to auditory stimuli (1 left anterior, 4 anterior, 3 right anterior, 2 right posterior, 11 posterior, 3 left posterior, 6 multidirectional), and 12 to both visual and auditory stimuli (1 left anterior, 1 anterior, 3 right anterior, 7 mul- tidirectional). The directional neurons tended to respond to visual stimulation pre- sented from the right anterior direction, and to auditory stimulation presented from posterior directions. Examples of directional responsiveness of 2 neurons that re- sponded to both visual and auditory stimuli were shown in Fig. 1A and Fig. 2A.

Of the 86 directional neurons, 62 were tested with more than 10 kinds of stimuli, and these could be divided into two subtypes. In one, responsiveness was indepen- dent of the nature of the stimulus (non-selective, n = 31). These non-selective neurons responded to several kinds of stimuli and sometimes to two modalities with almost same response magnitude. In the other, responsiveness depended on the nature of the stimulus and responded more to one or a few kinds of stimuli than to others (se- lective, n = 31). Examples of selective responsiveness of 2 neurons are shown in Figs. 1B and 2B. Many selective neurons (22/31) responded more strongly to human ac- tions such as walking than to other stimuli. Relations between subtypes and sensory modalities of directional neurons are shown in Table I.

The effects of direction of environmental cues were tested with 17 neurons by rotat- ing the chair in which the monkey was seated. Of these 17 neurons, the directional

295

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Fig. I. Example of visual- and auditory-selective egocentric neuron. A: strong directional responses to human walking at left. These responses were weakened but not extinguished when room lights were turned to reduce illumination off, when monkey was prevented, by opaque plates, from seeing human walking, and when stepping sounds were reduced or masked by white noise (not shown). Response latency to audi- tory stimuli, 180 ms. B: comparison of responses to various visual and auditory stimuli. This neuron tested with 11 visual stimuli and 10 auditory stimuli (not all results shown). It responded strongly to human movement, such as walking, and to manual presentation of spider model, apple, or stick. Broken line; spontaneous firing rate. C: directional responsiveness to human movement after animal was rotated 45 ° left from its initial position. Note that responsiveness to human movement at left (A) followed animal (C). Each arrow in A and C indicates direction of stimulus presentation. M shows position of monkey. Each histogram in A, B and C indicates mean and S.D. of three I s firing rate measurements after stimula- tion.

responsiveness of six remained constant relative to the monkey (egocentric neurons). An example of this type of neuron is shown in Fig. 1. The responsiveness to a human walking in various areas at the left side of the monkey, with the strongest response at the left anterior (Fig. 1A), stayed at the same position relative to the monkey when the monkey was rotated 45 ° to the left (Fig. 1C). The directional responsiveness of 4 neurons remained in place in the environment independent of the monkey's posi- tion (allocentric neurons). An example of this type of neuron is shown in Fig. 2. Re- sponsiveness to walking at the right anterior (Fig. 2A) remained fixed in the environ- ment and did not follow the monkey when the monkey was rotated 45 ° to the left

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Fig. 2. Example of visual- and auditory-selective allocentric neuron. A: directional responsiveness to hu- man walking. Note strong responses at right anterior. Response latency to auditory stimuli, 160 ms. B: comparison of responses to various visual or auditory stimuli. This neuron tested with 16 visual stimuli and 12 auditory stimuli (not all results shown), and responded to visual or auditory stimuli such as walking or standing up, apple approaching, clap, or crash. C: directional responsiveness to human walking (step sound) after animal was rotated 45 ° left from initial position. Note responsiveness to human walking at right anterior (A) remained fixed in environment when monkey was rotated (C). Other details as in Fig. l.

(Fig. 2C). The d i rec t ional responsiveness o f 7 o ther neurons ext inguished when the

m o n k e y was ro ta ted and reappeared when the m o n k e y was re turned to the initial

posi t ion.

The egocentr ic neurons are considered to code a di rect ion relat ive to the animal ,

whereas the a l locentr ic neurons code a fixed loca t ion in the envi ronment . In pr imates ,

including human, it has been suggested that the pref ronta l cor tex is i m p o r t a n t for

egocentr ic spat ial o r ien ta t ion whereas the infer ior par ie ta l lobule is impor t an t for

a l locentr ic spat ia l o r ien ta t ion [6, 15, 19]. These two cor t ical areas have ana tomica l

connect ions with the h i p p o c a m p u s via the p a r a h i p p o c a m p a l cort ices [1, 5, 20]. Thus,

the egocentr ic and al locentr ic responsiveness o f h i p p o c a m p a l neurons might reflect

inputs from the respective cort ical areas. It is not yet clear how h i p p o c a m p a l neurons

297

TABLE I

RELATIONS BETWEEN SENSORY MODALITIES, NON-SELECTIVE OR SELECTIVE SUB- TYPES, AND ALLOCENTRICITY OR EGOCENTRICITY OF DIRECTIONAL NEURONS

Numerals are number of neurons.

Visual Auditory Visual and Total (allocentric, (allocentric, auditory (allocentric, egocentric) egocentric) (allocentric, egocentric

egocentric)

Non-selective 18 10 3 31 (0, I) (0, 1) (0, 0) (0, 2)

Selective 9 16 6 31 (l, 2) (1, 1) (2, 1) (4, 4)

Total 27 26 9 62 (1, 3) (1, 2) (2, 1) (4, 6)

process spatial orientation. However, judging from the impairment of spatial memory by the hippocampal damage [3, 8, 12, 14, 18, 22], egocentric and allocentric neurons might be involved in storing, beyond the short term memory span, spatial relations between the location of the stimulus, the animal and other cues fixed in the environment.

The existence of non-selective and selective subtypes suggests their different func- tions. The non-selective subtype could reflect spatial attention, and the selective sub- type could reflect the association of a particular stimulus and a given direction (stim- ulus-direction association) to function in a memory process. Unit recording of mon- key hippocampal neurons that responded to combinations of information about the object and its position in object-place memory was recently reported [2, 17]. These neurons and the selective subtype neurons of our study were similar in that coded information about the property of a stimulus and its spatial contingency. There is no evidence to show why selective subtype neurons respond more to stimuli produced by human action than to other stimuli. However, it seems reasonable that responsive- ness might reflect the importance to the monkey of association between the experi- menter and the particular environment of the experimental room.

Anatomical studies suggest that the entorhinal cortex receives inputs both directly, and indirectly via the parahippocampal cortices, from both visual and auditory asso- ciation cortices [1, 5, 20], which are considered to be involved in analysis of physical properties of stimuli [4, 16]; and from the inferior parietal lobule and prefrontal cor- tex [1, 5, 20], which are considered to be involved in analysis of spatial information [6, 15, 19]. It has also been reported that bilateral lesions of the hippocampal forma- tion impaired performance in a spatial memory task [14] and a conditional spatial task [3], both of which required object-place association. We can thus imagine that association between a stimulus and its location either egocentric or allocentric space, as reflected in responses of the selective subtype, is formed in the hippocampal forma- tion.

298

We thank Dr. L.R. Squire, Universi ty of California, San Diego, and Dr. A. Simp-

son, Showa Universi ty, Tokyo, for critical comments and suggestions, and for help

in prepar ing this manuscr ipt . This research was part ly supported by the Japanese

Minis t ry of Educat ion , Science and Culture, Gran t s - in -Aid for Scientific Research,

634801 15, by a Bioscience G r a n t for In te rna t iona l Joint Research Project from the

N E D O , Japan, in 1989, and by Nissan Science F o u n d a t i o n in 1989.

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