Vibrissal coding in hippocampus

From Scholarpedia

Author: Prof. Antonio Pereira, Universidade Federal do Rio Grande do Norte/Edmond and Lily Safra International Institute of Neuroscience of Natal, Brazil
Author: Prof. Miguel A. L. Nicolelis, Duke University, NC, USA

Dr. Antonio Pereira accepted the invitation on 17 August 2009 (self-imposed deadline: 17 February 2010).

Dr. Antonio Pereira, Universidade Federal do Rio Grande do Norte, Edmond and Lily Safra International Institute of Neuroscience of Natal , Natal, Brazil, was invited on 17 August 2009.

Contents 1 Somatosensory pathways 2 Coding the location and identity of objects in somatosensory pathways 3 Anatomical overview of the hippocampus 4 The hippocampus and the cognitive map 5 Other theories of hippocampal function 6 The hippocampus as a novelty detector 7 Sensory inputs to the hippocampus 8 References

Somatosensory pathways

The spatial and temporal resolution of sensory percepts is greater when animals use active sensing systems, including echolocation in bats, electrolocation in some fish and haptic systems, such as the whisker array, in rodents and other animals (e.g. seals, manatees, etc.). Active haptic sensing with the whiskers in rats, for instance, consists of repeated posterior–anterior sweeps of the whiskers, moving synchronously, together with the head (Grant et al., 2009). Many rodents, being nocturnal animals, rely heavily on touch to navigate the environment and identify nearby objects, walls, and negotiate obstacles (Brecht et al., 1997). The whiskers, or vibrissae, are associated with sinus hair follicles, and innervated by the infraorbital nerve, a branch of the maxillary nerve (Dörfl, 1985). The follicle-sinus complex (FSCs) is a sophisticated tactile receptor contacted by about 200 cells from the trigeminal ganglion that can mediate very fine texture discrimination (Guic-Robles et al., 1989) and distance estimations (Krupa et al., 2001). The afferent signals continue along the central branch of the trigeminal ganglion to synapse onto the brainstem trigeminal nuclei (Jacquin et al., 1983). Vibrissal information then is transmitted fro trigeminal nuclei to the thalamus via parallel pathways up to the somatosensory cortex. In rats and mice, each major facial whisker is represented both functionally and anatomically by a discernible column arranged in a regular array along the primary somatosensory cortex (Welker and Woolsey, 1974; Pereira et al., 2001).

Coding the location and identity of objects in somatosensory pathways

Anatomical overview of the hippocampus

The hippocampal formation includes the dentate gyrus, the hippocampus proper, the subiculum, and the entorhinal cortex. The hippocampus is a three-layered cortical structure composed of subregions CA3, CA2, and CA1 (Amaral and Lavenex, 2007). The gateway to the hippocampal formation is the entorhinal cortex, which receives both unimodal and polymodal sensory inputs via the perirhinal and postrhinal cortices in rodents (Burwell and Amaral, 1998). Sensory inputs from the entorhinal cortex enter the hippocampus through the dentate gyrus (DG) and are relayed to CA3 and then to CA1, where it is processed and sent back to the entorhinal cortex via the subiculum. Entorhinal afferents can also be transmitted monosynaptically to the CA1 and CA3 subfields.

The hippocampus and the cognitive map

It has been consistently shown in rodents that the activity of pyramidal neurons in the CA1 and CA3 hippocampal subfields are highly correlated with the animal's spatial location (O’Keefe & Dostrovsky, 1971). For instance, a population of cell-specific ‘place fields’ could, in theory, be used to determine the animal’s location in the environment (Wilson & McNaughton, 1993). A place field is built on information derived from self-motion and perceptual information.Place cells are the main justificative for the cognitive-map theory of hippocampal function. According to it, the hippocampus´ primary role is to elaborate and store allocentric representations of locations in the environment to aid flexible navigation. In human patients with hippocampal damage, the pattern of spared and impaired cognitive processes, together with results from animal models of amnesia, has led to the Declarative Theory of hippocampal function (Squire et al., 2004). The predominantly spatial deficits seen in animal lesion studies, on the other hand, have largely supported the spatio–temporal context of human episodic memories.

Other theories of hippocampal function

Several theories regarding the role of the hippocampus in memory have been proposed over the years. Declarative theory; Multiple-trace theory; Dual-process theory; Relational theory. There is strong evidence that the mammalian hippocampus plays an important role in navigation as well, by creating a map-like, spatial representation of the environment. To be useful, however, this map needs to be constantly updated whenever some relevant feature changes in the outside world. Several studies have shown that the hippocampus and other structures in the medial temporal lobe are crucially involved with novelty detection. Novelty detection calls for a system that is able to hold detailed models of the environment and keep track of changes that violate specific predictions of this model. The hippocampal CA1 field provides just this type of system by comparing sensory inputs from the entorhinal cortex with information stored in the CA3 field.

The hippocampus as a novelty detector

hippocampus operates as a comparator during the processing of associative novelty, generating mismatch/novelty signals when prior predictions are violated by sensory reality.

Sensory inputs to the hippocampus

Surprisingly, however, despite the wealth of anatomical connections capable of bringing sensory inputs to the hippocampus, little is known about the processing of sensory signals other than vision.

References

• Amaral D., Lavenex P. 2007. Hippocampal Neuroanatomy. In The Hippocampus Book. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe, Eds., New York: Oxford University Press, pp. 37-114.

• Brecht M., Preilowski B., Merzenich M.M. 1997. Functional architecture of the mystacial vibrissae. Behav Brain Res 84:81–97.

• Burwell R.D., Amaral D.G. 1998. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol 398:179-205.

• Diamond M.E., von Heimendahl M., Knutsen P.M., Kleinfeld D., Ahissar E. 2008. ‘Where’ and ‘what’ in the whisker sensorimotor system. Nature Rev Neurosci 9:601-612.

• Dörfl J. 1985. The innervation of the mystacial region of the white mouse. A topographical study. J Anat 142: 173-184.

• Fox C., Humphries M., Mitchinson B., Kiss T., Somogyvari Z., Prescott T. 2009. Technical integration of hippocampus, basal ganglia and physical models for spatial navigation. Front Neuroinform (2009) 3:6. doi: 10.3389/neuro.11.006.2009.

• Grant R.A., Mitchinson B., Fox C.W., Prescott T.J. 2009. Active Touch Sensing in the Rat: Anticipatory and Regulatory Control of Whisker Movements During Surface Exploration. J Neurophysiol 101:862-874.

• Guic-Robles E.C., Valdivieso C., Guajardo G. 1989. Rats can learn a roughness discrimination using only their vibrissal system. Behav Brain Res 31:285–289.

• Jacquin M.F., Semba K., Egger M.D., Rhoades R.W. 1983. Organization of HRP-labeled trigeminal mandibular, primary afferent neurons in the rat. J Comp Neurol 215:397-420.

• Krupa D.C., Mattel M.S., Brisben A.J., Oliveira L.M., Nicolelis M.A.L. 2001. Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J Neurosci. 21:5752-5763.

• Kumaran D., Maguire E.A. 2006. An unexpected sequence of events: Mismatch detection in the human hippocampus. PLoS Biol 4(12): e424. DOI: 10.1371/journal.pbio.0040424

• O'Keefe L., Dostrovsky J. 1971. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely moving rat. Brain Res 34:171–175.

• Paz-Villagrán V., Save E., Poucet B. 2006. Spatial discrimination of visually similar environments by hippocampal place cells in the presence of remote recalibrating landmarks. Eur J Neurosci 23:187-195.

• Pereira A., Freire M.A.M., Bahia C.P., Franca, J.G., Picanço-Diniz, C.W. 2001. The barrel field of the adult mouse Sml cortex as revealed by NADPH-diaphorase histochemistry. Neuroreport 11:1889-1892.

• Squire L.R., Stark C.E., Clark R.E. 2004. The medial temporal lobe. Annu Rev Neurosci. 27:279–306.

• Suzuki W.A., Amaral D.G. 1994. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J Comp Neurol 350:497-533.

• Welker C., Woolsey T.A. 1974. Structure of layer IV in the somatosensory neocortex of the rat: Description and comparison with the mouse. J Comp Neurol 158:437–453.

• Wilson M.A., McNaughton B.L. 1993. Dynamics of the hippocampal ensemble code for space. Science 261:1055–1058.

Invited by:

Prof. Tony J. Prescott, Dept Psychology, Univ of Sheffield, UK