Research reportImplicit coding of location and direction in a familiar, real-world “vista” space
Introduction
To be oriented in the world, many animals, including humans, rely on an accurate representation of one’s spatial position and facing direction. Previous neurophysiological experiments demonstrated the neuronal signature of these information by means of place and head-direction cells. Indeed, “place cells” in the hippocampus fire whenever the animal is at a particular location [1], determined by the geometry of the environment [2], independently from the direction of the animal’s head and from where it is looking at; “head-direction cells” in Papez circuit structures fire only when the animal maintains a certain heading or orientation within the environment [3], [4], independently from its location and from where it is looking at.
In humans, neuroimaging and behavioral evidence revealed the existence of a direction-dependent and location-dependent spatial representation. By using a small-scale, fully controlled, virtual reality environment, we recently showed that the parahippocampal place area (PPA) and the retrosplenial complex (RSC) automatically encode one’s own location and orientation during the exposure to a familiar environment [5] and that these information have a map-like organization, with closer physical locations entailing activity patterns more similar in neural representational space. On the other side, by using a large-scale, familiar real-world environment, Vass and Epstein [6] showed that activity patterns in RSC, left presubiculum and medial parietal cortex contain information about location but not about heading, which was instead represented in the right presubiculum. Additionally, they found behavioral priming effects when either view or location was repeated on successive trials, even when individuals were performing a directional task. Imagined location and imagined facing direction within a newly learned, small-scale virtual environment have been further explored in a recent study [7] using a judgment of relative direction (JRD) task, which required subjects to imagine themselves in a specific location and facing a specific direction. The authors found that reaction times were speeded when imagined facing direction or imagined location was repeated across consecutive trials.
The existence of a direction-dependent representation has also been demonstrated by using spatial memory tasks. For example, in recent experiments from our laboratory [8], [9] we found that performance in remembering object location from different views was faster and more accurate when facing direction on the visual scene is known in advance. Previous behavioral research on spatial memory recall (reviewed in [10]) has also reported orientation-dependent performance. For example, the geometry of the enclosing room, and more specifically alignment with the room walls, influenced how adults mentally represent space [11] and participants were faster and more accurate when asked to recall object location from a particular orientation [12].
Taken together, these pieces of evidence represent an important step toward understanding how location and direction are represented in the human brain, but leave many questions unanswered. Although the above-mentioned studies have provided strong support for the existence of location- and direction-dependent spatial representations, the experimental settings are so radically different that further investigations are needed. For example, some studies have frequently used room-sized (e.g., [13], [14], [15]) or table-top (e.g., [16], [17], [18]) displays in real context with the aim to control exposure to specific orientations and limit the participant’s movement. In such situations, the whole display can be viewed within a glimpse, with small head or trunk movements (i.e., “vista” space; [19], [20]). Other studies have used large-scale real environments [6], [21], [22], [23] or large virtual spaces [7], [18], in which different locations are not simultaneously in view (i.e., “environmental” space; [19], [20]) but can be experienced only if the observer moves through the environment.
Thus, the distinction between “vista” and “environmental” spaces seems to be relevant in the context of navigation, although the impact of different spatial scales on spatial representations has been rarely considered. It is also possible that some “vista” spaces, such as town squares, are substantially different from room-sized environments since they are more navigationally relevant, being more directly connected with the surrounding environmental space (for example, through streets that links the square with a neighboring place located beyond the sensory horizon).
The present study was designed to test whether spatial representation of one’s own location and facing direction within a familiar outdoor “vista” space reveal the same organization observed in more-controlled room-sized virtual (and real) environments and in large-scale environmental spaces. We hypothesized that locations and facing directions are implicitly encoded, even in the absence of a navigational task or of an explicit requirement to encode these spatial quantities. We test this hypothesis by asking participants to perform the explicit encoding of either of two spatial dimensions (their own position or their facing direction) on a series of pictures taken from a real familiar square, while the other, task-irrelevant, dimension (i.e., their facing direction or their own position) was implicitly repeated across consecutive trials. By analysing data as a function of repetition of the task-irrelevant information, we expected to found a behavioral advantage (priming effect) when positions and facing directions were repeated across trials, even in absence of any explicit demand to encode either of them. Since previous studies reported distinct neural patterns for position- and facing direction-representations [5], [6], we also hypothesized that the behavioral advantage for repeated trials should be different for position and facing direction, indicating that representing of one’s own direction is substantially different from representing of one’s own location.
We further explored differences between position and facing direction representations by looking at potential gender effects. Several studies reported gender differences in spatial cognition [24], [25] and the use of different strategies during spatial tasks, with males more likely than females to use a survey strategy [26], [27]. Based on this evidence, we hypothesized that females are more likely influenced by directional information on how paths connect different landmarks, while males mainly rely on a global spatial representation allowing them to ascertain the correct position, based on a route- and body-independent (allocentric) retrieval [28]. In particular, we hypothesized that females show different priming effects for repeated positions and directions, showing a preference for direction-dependent rather than position-dependent priming effects. Finally, inspired by our previous study showing map-like representations for positions and facing directions in a small scale virtual room [5], we explored whether these spatial quantities are represented topographically even in a real-world “vista” space, with closer physical locations/directions entailing different behavioral patterns. To test this hypothesis, we analyzed data as a function of real distances between consecutive positions/directions.
Section snippets
Subjects
Thirty neurologically normal volunteers (15 females, mean age 25, SD 3.4; t1,29 = 0.94; p = ns) participated to the study. The neurological status of each volunteer was assessed thought a clinical interview and an informal anamnesis. All subjects were students at the Sapienza University of Rome (16 years of education on average). All subjects were right handed, as assessed by the Edinburgh Handedness Inventory [29], and had normal or corrected-to-normal vision. The study was approved by the local
Priming effects for position and direction
After reaching a criterion during the training phase in which they were required to consolidate their knowledge about a familiar place, participants were tested on their ability to explicitly encode their own position (Position Task or PT) or facing direction (Direction Task or DT) on a sequence of snapshots taken from this place. Across consecutive trials, in half of the cases the facing direction was repeated in PT, and the observer’s position was repeated in DT. We hypothesized that an
Discussion
In the current study we found that navigationally relevant information, such as place information about where we stand in a real, familiar environment, and directional information about which orientation we are facing at, are automatically encoded even in the absence of any explicit navigational task. One key aspect of our paradigm is, indeed, that participants were engaged in a spatial task that is independent from the studied representations, so that the specific effects we described are to
Acknowledgements
The present study was supported by funding from Sapienza University of Rome to VS (Avvio alla Ricerca, 2015; nr C26N15424T) and by the Italian Ministry of Health — Fondazione Santa Lucia (RC2014-2016) to GG. We thank Nicole Civale for reviewing the English style.
References (49)
Head direction cells and the neurophysiological basis for a sense of direction
Prog. Neurobiol.
(1998)- et al.
Role of the human retrosplenial cortex/parieto-occipital sulcus in perspective priming
Neuroimage
(2016) Spatial memory: how egocentric and allocentric combine
Trends Cogn. Sci.
(2006)- et al.
Systems of spatial reference in human memory
Cogn Psychol
(2001) - et al.
Spatial abilities at different scales: individual differences in aptitude-test performance and spatial-layout learning
Intelligence
(2006) The assessment and analysis of handedness: the Edinbourgh Inventory
Neuropsychologia
(1971)- et al.
Cognitive maps in imagery neglect
Neuropsychologia
(2012) - et al.
One’s own country and familiar places in the mind’s eye: different topological representations for navigational and non-navigational contents
Neurosci. Lett.
(2014) - et al.
Matching categorical object representations in inferior temporal cortex of man and monkey
Neuron
(2008) - et al.
Visuospatial working memory and changes of the point of view in 3D space
Neuroimage
(2007)
Gender differences in spatial orientation: a review
J. Environ. Psychol.
Perspective changing in primary and secondary learning: a gender difference study
Learn. Individ. Differ.
The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat
Brain Res.
Geometric determinants of the place fields of hippocampal neurons
Nature
Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation
Exp. Brain Res.
Distributed cognitive maps reflecting real distances between places and views in the human brain
Front. Hum. Neurosci.
Abstract representations of location and facing direction in the human brain
J. Neurosci.
Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe
Nat. Neurosci.
Visuospatial transformations and personality: evidence of a relationship between visuospatial perspective taking and self-reported emotional empathy
Exp. Brain Res.
Multiple views of spatial memory
Psychon. Bull. Rev.
Intrinsic frames of reference in spatial memory
J. Exp. Psychol. Learn. Mem. Cogn.
Micro- and macroreference frames: specifying the relations between spatial categories in memory
J. Exp. Psychol. Learn. Mem. Cogn.
Layout geometry in the selection of intrinsic frames of reference from multiple viewpoints
J. Exp. Psychol. Learn. Mem. Cogn.
Mental representations of large and small spatial layouts are orientation dependent
J. Exp. Psychol. Learn. Mem. Cogn.
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