Research Article

Spatial Representation in the Entorhinal Cortex

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Science  27 Aug 2004:
Vol. 305, Issue 5688, pp. 1258-1264
DOI: 10.1126/science.1099901
  • Fig. 1.

    Topographic projections from MEC to hippocampus. (A) Ventral-posterior view of a whole rat brain showing the outline of the left entorhinal cortex (colored surface) and the rhinal fissure (stippled gray line). The dorsolateral-to-ventromedial gradient of entorhinal extrinsic connectivity (magenta-to-blue) cuts across both lateral and medial entorhinal subdivisions (border indicated by yellow line). Filled white markers indicate sites of tracer injection in (B) and (C). Open white markers indicate injections not illustrated. Filled yellow markers show recording positions in Figs. 2A, 3A, 3C, and 5E. Open yellow markers indicate selected additional recording positions in MEC. (B) Sagittal sections illustrating the projections from the dorsolateral-band zone of MEC to the hippocampus. (Left) Injection site of BDA. Dorsal and ventral borders of MEC are indicated by red lines. (Middle) Low-power brightfield sagittal section showing dense staining in dorsal but not ventral hippocampus (black arrowheads indicate borders between hippocampal subfields). (Right) High-power darkfield photomicrographs of indicated areas in the dorsal and ventral hippocampus. (Top right) Bright orange band corresponds to dense labeling in the middle molecular layer of the dentate gyrus (red arrow) (21). The labeling more dorsally (yellow arrow) corresponds to the less massive termination of MEC fibers in the proximal half of CA1. (C) Projections from the ventromedial region of MEC. Note the absence of staining in dorsal hippocampus (darkfield picture, top right) and moderate labeling in fields CA1 and dentate gyrus of the ventral hippocampus (darkfield picture, bottom right; yellow and red arrows, respectively) (21).

  • Fig. 2.

    Discrete multipeaked firing fields in putative excitatory cells in the dorsolateral band of MEC. (A) Nissl stain showing electrode locations in layers III (upper red circle) and II (lower red circle) of the dorsolateral band (sagittal section; see also Fig. 1A). Red lines indicate borders of MEC toward postrhinal cortex (dorsal) and parasubiculum (ventral). (B) Firing fields of simultaneously recorded cells from the lower location in (A). Each row shows one cell, and each pair of columns one trial. The trajectory with superimposed spikes (red) is shown to the left in each pair of columns; the corresponding color-coded rate map (with the peak rate) appears to the right. The color scale is linear with blue as zero and red as maximum. Regions not covered by the rat are in white. Note the multiple discrete firing fields that were stable across trials. (C) Trajectory maps and color-coded maps showing similar fields for each directional quadrant of body movement for three of the cells in (B). (D) Distance between neigboring firing fields in dorsolateral-band cells with more than two fields (all rats; mean, SEM, and range for each cell). Red lines indicate chance level.

  • Fig. 3.

    Weak spatial modulation in the intermediate band (A) and absence of spatial modulation in the ventromedial band (C) of MEC. Sagittal sections indicating recording locations of layer II in the intermediate band [red circles in (A)] and in layers III and II of the ventromedial band [upper and lower red circles in (C), respectively] (see also Fig. 1A). Borders of MEC are indicated by red lines. (B and D) Firing fields of simultaneously recorded cells in layer II of the intermediate or ventromedial band [(B) and (D), respectively].

  • Fig. 4.

    Spatial modulation in superficial layers of MEC compared to hippocampal area CA1. (A and B) Color-coded rate maps and trajectory maps for cells recorded simultaneously from layer II in the dorsolateral band (A) and dorsal CA1 of the contralateral hippocampus (B). Each column shows one cell. The top two rows show trial 1; the bottom two rows show trial 2. (C to K) Quantitative analysis of spatial modulation in putative excitatory cells of layers II and III in dorsolateral, intermediate, and ventromedial bands of MEC as compared to pyramidal cells in dorsal CA1 (all cells in all regions). Panels show distribution of average rate (C), peak rate (D), number of fields (E), mean field size (F), sparsity (G), spatial coherence (H), spatial information rate (I), stability (J), and modulation by movement direction (K) (21, 23).

  • Fig. 5.

    Spatial firing in the dorsolateral band may reflect intrinsic computations of the MEC. (A to D) Spatial modulation in the dorsolateral band of MEC in two rats with ibotenate lesions of the hippocampus (three sagittal levels from lateral to medial). The rat in (A) and (B) had a complete lesion of CA3, CA1, dentate gyrus, and subiculum; the one in (C) and (D) had a complete lesion of CA3 and CA1, but dentate gyrus and subiculum were partly spared. Red circles indicate electrode locations in layer II; red lines indicate borders of MEC. Both animals had cells with discrete multipeaked firing fields, but the coherence of the fields was reduced. (E to H) Absence of strong spatial modulation upstream in adjacent postrhinal cortex. (E) Sagittal section through the postrhinal cortex (POR) and MEC indicating recording locations (red circles) and regional borders (parasubiculum, PaS; presubiculum, PrS; see also Fig. 1A). Note that two recording locations were in POR (layers V and III) and one in MEC (layer III). (F and G) Dispersed and unstable firing fields of postrhinal broadwaveform cells at the upper (F) and lower (G) recording position in POR. (H) Multiple discrete firing fields in a layer-III neuron at the succeeding recording position in MEC.

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  • Abstract
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    Spatial Representation in the Entorhinal Cortex
    M. Fyhn, S. Molden, M. P. Witter, E. I. Moser, M.-B. Moser

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      Example of 20 second Bayesian decoding of the ensemble activity of 8 simultaneously recorded principal neurons in the dorsolateral band of MEC in a rat running in a square box (1 x 1 m). The actual location of the rat is indicated by a red cross. The trajectory of the rat was predicted using place fields constructed from an independent set of the data (see Materials and Methods in Supplementary Online Material). The blue dots are samples from the prediction probability distribution. High density of dots indicates high conditional probability of finding the rat at that particular location. The green dots are samples from a null model, which is a simulation of the same random walk assumed by the decoding algorithm, except that the neural activity is ignored. Note that the predictive distribution is mostly unimodal with a difference between the mode of the predictive distribution and the rat's actual path of ~ 5-10 cm. The unimodality is interrupted by short periods with multiple modes at 3-4 sec, 10-12 sec, and 17-20 sec, reflecting the periodic influence of more than one peak in the firing field when the sample size is limited.

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