Spatial Memory in Humans

Mitul A. Mehta

Centre for Neuroimaging Sciences, Institute of Psychiatry at King's College London, London, uK


Spatial memory is often used to describe spatial navigation and encompasses egocentric and allocentric memories


Spatial memory describes information storage and retrieval required for identification and navigation of proximal or distal space. This is distinct from spatial working memory which refers to active representations stored and manipulated over seconds. Two main frames of reference have been described: egocentric, which is related directly to the observer, and allocentric, which is dependent on the relational position of objects in space. Routes depend more on egocentric frames of reference, whereas maps are more flexible to landmark changes and thus depend more on allocentric frames of reference. Although often discussed separately, an emerging view is that both egocentric and allocentric spatial memories are coded but these may interact and depend on interacting brain regions. Spatial memories can be representations of salient cues for navigation or be more detailed representations, including topography, allowing reexperiencing of the environment (Moscovitch et al. 2005). A useful analogy has been proposed such that schematic representations of topography correspond to ► semantic memory and detailed representations correspond to ► episodic, autobiographical memory. Classic tasks of spatial memory in experimental animals include the ► Morris water maze, Olton maze, and ► radial arm maze (although these latter tasks can incorporate a large ► working memory component). In humans, both static (route reporting and drawing) as well as real-world tasks can be used and while being informative, they are severely limited in interpretability and control of motivation and strategy. Emerging use of virtual reality provides a mechanism to integrate realistic representations of space and environment with controlled laboratory assessments, including functional brain imaging, which requires the participant to remain still during the course of an experiment.

Functional Neuroanatomy

The human visual system comprises two processing streams, a dorsal "where" system important for spatial navigation and a ventral "what" system for object recognition. Goodale and Milner (1992) emphasized the transformations that may be required for information in each stream, relabeling the dorsal stream as a ''how'' system. This system was proposed to be involved in action preparation via transformation of visual information using an egocentric frame of reference, whereas the ventral system processed transformation for long-lasting representations using multiple frames of reference. Functional brain imaging, including studies using virtual reality, largely supports this general distinction. For example, Aguirre and D'Esposito (1997) initially trained subjects on learning the location of 16 objects in a virtual town. ► Functional MRI (fMRI) scanning was performed during two conditions in which they judged (1) if the appearance of a location within the town matched the name of a location -the appearance condition; or (2) the direction of travel from a displayed location in the town to a given new location - the position condition. When contrasted against each other, the appearance condition showed greater activation in the fusiform and parahippocampal gyrus as well as occipital regions, whereas the position condition showed greater activation in more dorsal areas (i.e., superior and inferior parietal lobes). This study was performed in only four volunteers, but in general there is an agreement that the ► hippocampus and medial temporal lobe structures are required for the acquisition of spatial memories in humans (Parslow et al. 2005) and while fewer studies have examined retention and retrieval of spatial memories, the results of the ► fMRI study fit with studies showing that detailed episodic spatial memories cannot survive damage to the hippocampus/medial temporal lobe (Moscovitch et al. 2005) and retrieval of spatial memories of taxi drivers in London activates hip-pocampus/parahippocampal gyrus (Maguire et al. 1997). An alternate view is that the hippocampus may not have a selective role in allocentric spatial memory. For example, in a group of six patients with hippocampal damage performing an image-location memory task, impairments were dependent on the number of items rather than the degree of rotation between study and test phases (Shrager et al. 2007), although the use of smooth rotation might have favored egocentric mental rotation strategies (Burgess 2008).

Overall, these studies align with the presence of hippocampus ► place cells in the rodent, monkey, and human brain. In humans, these cells were first described in seven patients with intractable epilepsy undergoing presurgical invasive monitoring, who played the role of a taxi driver in a spatial navigation game (Ekstrom et al. 2003). Cells that responded to specific locations were primarily located in the hippocampus, whereas cells that responded to views of landmarks were primarily located in the parahippocampal region. Indeed, forming memories of places, or landmarks or associating objects with particular locations, appears to require the parahippo-campal cortex. Other extrahippocampal regions also important for spatial memory task performance include the posterior parietal cortex and striatum. The former is necessary in the representation of spatial information in terms of egocentric coordinates, allowing reaching and movement plans to be formulated as well as egocentric imagery. The striatum is generally thought to have a role in the learning of the procedural aspects of tasks, and may have dissociable roles in egocentric and allo-centric spatial memory consolidation (De Leonibus et al. 2005). Using a task of object exploration with animals entering the same location (egocentric reference frame) or different locations (allocentric reference frame), focal injection of an NMDA receptor antagonist into the dorsal striatum impaired consolidation of the egocentric procedure, whereas intra-accumbens administration impaired both procedures.

Impact of Psychoactive Drugs

In experimental animals, the neurobiology and psycho-pharmacology of spatial memory have been extensively studied, dominated by the use of the Morris water maze (McNamara and Skelton 1993). The neurotransmitter and molecular mechanisms of medial temporal lobe and cortical structures involved in spatial memory implicate specific drug systems in the accurate acquisition and expression of these memories. Focusing on the hippocampus as the most studied of these regions implicates glutamergic neurotransmittion through ► AMPA and ► NMDA receptors, as well as modulatory influences of the cholinergic and serotonergic inputs. Muscarinic and nicotinic cholinergic receptor blockade as well as serotonin receptor antagonism can all modulate hippocampal glu-tamatergic and ► GABAergic neurotransmission as well

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