Neural and Behavioural Correlates of Human Navigation

Oliver Baumann

My research concerns the cognitive processes and neural circuits that underlie our ‘sense of direction’ and the distinct processes of memory encoding and retrieval during active navigation through three-dimensional space. The research methods used include the assessment of behavioural performance as well as neuroimaging techniques.

In our initial experiment (Baumann, Chan & Mattingley, Neuroimage, February 1, 2010) we sought to identify the neural circuits that underlie the distinct processes of encoding and retrieval during landmark-based navigation. We used functional magnetic resonance imaging (fMRI) to measure neural responses as participants learned the location of a single target object relative to a small set of landmarks. Following a delay, the target was removed and participants were required to navigate back to its original position (Figure 1).

Schematic of the virtual environment used in the navigation task

 

Figure 1: Schematic of the virtual environment used in the navigation task.

 

 

 

 

 

At encoding, greater activity within the right hippocampus and the parahippocampal gyrus bilaterally predicted more accurate navigation to the hidden target object in the retrieval phase. By contrast, during the retrieval phase, more accurate performance was associated with increased activity in the left hippocampus and the striatum bilaterally. Dividing participants into good and poor navigators, based upon behavioural performance, revealed greater striatal activity in good navigators during retrieval, perhaps reflecting superior procedural learning in these individuals. By contrast, the poor navigators showed stronger left hippocampal activity, suggesting reliance on a less effective verbal or symbolic code by this group (Figure 2).

Magnetic resonance brain slices

 

Figure 2: Magnetic resonance brain slices showing mean functional activity from the analysis comparing good and poor navigators during the retrieval phase. Good navigators showed stronger activity in two regions. (a) Left striatum. (b) Right striatum. Poor navigators showed stronger activity in a single region. (c) Left hippocampus

 

 

 

 

 

 

Our findings suggest separate neural substrates for the encoding and retrieval stages of object location memory during active navigation, which are further modulated by participants' overall navigational ability.

Another cognitive function, crucial for successful navigation, is the ability to encode and update representations of heading direction. In rats, head-direction cells located within the limbic system alter their firing rate in accordance with the animal's current heading. However until now, the neural structures that underlie an allocentric or viewpoint-independent sense of direction in humans remained unknown. The goal of our second study (Baumann & Mattingley, The Journal of Neuroscience, September 29, 2010) was therefore to identify brain regions that are modulated by learned heading. We used functional magnetic resonance imaging to measure neural adaptation to distinctive landmarks associated with one of four heading directions in a virtual environment. Our experiment consisted of two phases: a "learning phase," in which participants actively navigated the virtual maze; and a "test phase," in which participants viewed pairs of images from the maze while undergoing fMRI (Figure 3).

Schematics

Figure 3: Schematics of the virtual environment used to examine the representation of allocentric heading. (a) Aerial perspective of the virtual maze used in the learning phase. The red dots indicate the locations of the 20 symbols that acted as landmarks; The arrows represent the 16 different vantage points from which participants viewed the landmarks during the test phase. (b) Example of a single image viewed by participants during the test phase.

We found that activity within the medial parietal cortex—specifically, Brodmann area 31—was modulated by learned heading, suggesting that this region contains neural populations involved in the encoding and retrieval of allocentric heading information in humans (Figure 4).

Magnetic Resonance Image of an MNI-normalized brain

 

Figure 4: A magnetic resonance image of an MNI-normalized brain that shows heading-direction-selective activity in the left medial parietal cortex

 

 

 

 

 


These results are consistent with clinical case reports of patients with acquired lesions of medial posterior brain regions, who exhibit deficits in forming and recalling links between landmarks and directional information. Our findings also help to explain why navigation disturbances are commonly observed in patients with Alzheimer's disease, whose pathology typically includes the cortical region we have identified as being crucial for maintaining representations of heading direction.

In our most recent research study (Baumann, Chan & Mattingley, 2012) we place particular emphasis upon the distinct neural circuits that underlie categorical and coordinate representations of object locations, an aspect of human navigation ability that has to date been neglected in the field. It had been proposed that spatial landmarks are encoded either categorically, such that the relative positions of objects are defined in prepositional terms (e.g., to the left/right, in front/behind, etc.); or in terms of visual coordinates, such that the precise distances between objects are represented. In humans, it has been assumed that categorical representations are subserved by a left hemisphere neural network, whereas coordinate representations are largely right-lateralised. However, evidence in support of this distinction has been garnered almost exclusively from tasks that involved static, two-dimensional arrays (e.g., objects arranged on a table-top), rather than in the context of active navigation. In the present study, we used functional magnetic resonance imaging (fMRI) to identify neural circuits underlying categorical and coordinate representations during active spatial navigation of a fixed, virtual environment. In the encoding phase of each trial, participants navigated to the location of a target object and encoded either its spatial quadrant relative to a reference landmark (Categorical condition) or its distance from a reference landmark (Coordinate condition). After a short delay, participants re-entered the arena and were required either to navigate back to the appropriate quadrant of the arena, disregarding their distance from the landmark, or to navigate to an appropriate distance from the landmark ignoring the quadrant. We examined fMRI activity patterns during the encoding period, during which visual exposure to the virtual environment was matched across conditions. Activity in the categorical versus coordinate condition was significantly greater in the posterior and medial parietal cortex bilaterally, and in the left middle temporal gyrus. The complementary contrast (coordinate minus categorical) revealed greater activity in the right hippocampus, parahippocampus and dorsal striatum. These findings are broadly consistent with analogous studies in rodents, and support the suggestion of distinct neural circuits underlying categorical and coordinate representations of object location during active spatial navigation. Our results provide novel insights into how humans acquire and store knowledge about spatial relations between locations and objects while actively navigating through three-dimensional space.

We are currently finalizing a series of follow-up studies, with the aim to investigate further aspects of how humans use, process and memorize landmarks for spatial navigation. Our aim is to gain a comprehensive understanding of the fundamental properties of objects as landmarks, the cognitive processes involved in the identification and storage of these landmarks, and its ultimate effect on human navigation.

Publications

  • Baumann, O., Chan E., Mattingley J.B. (2012) Distinct neural networks underlie encoding of categorical versus coordinate spatial relations during active navigation. NeuroImage.
  • Baumann O., Skilleter A. & Mattingley J.B. (2011) Short-term Memory Maintenance of Object Locations during Active Navigation: Which Working Memory Subsystem is Essential? PLoS One.  (PDF File 202 KB)
  • Baumann, O., Mattingley J.B. (2010b) Medial parietal cortex encodes perceived heading direction in humans. Journal of Neuroscience 30: 12897-12901.   (PDF File 692 KB) 
  • Baumann, O., Mattingley, J.B. (2010a) Scaling of neural responses to visual and auditory motion in the human cerebellum. Journal of Neuroscience 30: 4489-4495.   (PDF File 466 KB)
  • Baumann O., Chan, E., Mattingley, J.B. (2010) Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans. NeuroImage 49:2816-2825.   (PDF File 1,035 KB)
  • Magnussen, S., Greenlee, M.W., Baumann, O., Endestad, T. (2010) Visual perceptual memory - anno 2008. In: Memory, aging and the brain. Bäckman L, Nyberg L, eds. London: Psychology Press.
  • Baumann, O., Belin, P. (2010) Perceptual scaling of voice identity: common dimensions for different vowels and speakers. Psychological Research 74: 110-120.   (PDF File 200KB)
  • Baumann, O., Greenlee, M.W. (2009) Effects of attention to auditory motion on cortical activations during smooth pursuit eye tracking. PLoS ONE 4(9): e7110. doi:10.1371/journal.pone.0007110   (PDF File 255 KB)
  • Baumann, O., Endestad, T., Magnussen, S., Greenlee, M.W. (2008) Delayed discrimination of spatial frequency for gratings of different orientation: behavioral and fMRI evidence for low-level perceptual memory stores in early visual vortex. Experimental Brain Research 188:363-369.  (PDF File 303 KB)

Submissions

  • Baumann, O., Mattingley J.B. Functional topography of primary emotion processing in the human cerebellum (submitted)
  • Chan, E., Baumann, O., Bellgrove, M., Mattingley J.B. Reference frames in allocentric representations are invariant over time and encoding perspective (submitted)
  • Chan, E., Baumann O., Bellgrove, M., Mattingley J.B. Extrinsic reference frames modify the neural substrates of object-location representations (submitted)
  • Chan, E., Baumann O., Bellgrove, M., Mattingley J.B. Negative emotion during navigation enhances parahippocampal place memory (submitted)
  • Chan, E., Baumann O., Bellgrove, M., Mattingley J.B. From objects to landmarks: The function of visual information in spatial navigation (submitted)

Conference Abstracts

  • Baumann O. Chan E. & Mattingley J.B. (2011) Neural correlates of categorical and coordinate encoding of object locations during active navigation. 11th Annual Meeting of Vision Sciences Society, Naples, USA.
  • Baumann O. Chan E. & Mattingley J.B. (2011) Extrinsic reference frames modify the neural encoding of object locations during active spatial navigation. 11th Annual Meeting of Vision Sciences Society, Naples, USA.
  • Greenlee MW, Frank SM, Baumann O & Mattingley JB (2011) fMRI correlates of visual-vestibular interactions in self motion perception. European Conference for Visual Perception, Toulouse, France.
  • Baumann, O., Mattingley J.B. (2010) Retrosplenial cortex encodes heading direction in humans. Human Brain Mapping Meeting, Barcelona, Spain, June.
  • Baumann, O., Mattingley, J.B. (2010) Scaling of neural responses to visual and auditory motion in the human cerebellum. Human Brain Mapping Meeting, Barcelona, Spain, June.
  • Baumann, O., Mattingley, J.B. (2010) Retrosplenial cortex encodes heading direction in humans. 37th Australasian Experimental Psychology Conference, Melbourne, April.
  • Chan, E., Baumann, O., Bellgrove, M., Mattingley, J.B. (2010) The influence of environmental cues on the formation of object-location representations within a virtual environment. 37th Australasian Experimental Psychology Conference, Melbourne, April.
  • Baumann, O., Chan, E., Mattingley, J.B. (2009) Hippocampal, parahippocampal and striatal neuronal activity predicts object-location retrieval during active navigation. 9th Conference of the Australasian Society for Cognitive Science, Sydney, September.
  • Chan, E., Baumann, O., Bellgrove, M., Mattingley, J.B. (2010) The influence of environmental cues on the formation of object-location representations within a virtual environment. 9th Conference of the Australasian Society for Cognitive Science, Sydney, September.
  • Baumann, O., Chan, E., Mattingley, J.B. (2009) Hippocampal, parahippocampal and striatal activity predicts object-location recall during active navigation. Cognitive Neuroscience Society Annual Meeting, San Francisco, USA, March.
  • Baumann, O., Endestad, T., Magnussen, S., Greenlee, M.W. (2008) Perceptual memory representations studied in delayed discrimination of spatial frequency - behavioral and fMRI evidence for high-fidelity visual stores in early visual cortex. Human Brain Mapping Meeting, Melbourne, June.
  • Baumann, O., Endestad, T., Magnussen, S., Greenlee, M.W. (2008) Delayed discrimination of spatial frequency for gratings of different orientation: behavioral and fMRI evidence for low-level perceptual memory stores in early visual. Cognitive Neuroscience Society Annual Meeting, San Francisco, USA, April.

Ongoing Collaborative Research

GO8-DAAD Collaboration with Prof. Mark W. Greenlee at the University of Regensburg. Project Title: Visual-Vestibular Interactions for active navigation and spatial object-location memory.

Collaboration with Paul Stockwell and Andrew Smith: The study seeks to compare the algorithmic techniques for generating concept maps against those created by humans.

Other activities outputs

Research Australia Griffith Discovery Award (2011)

Media Coverage

 

The Influence of Alignment on Object-Location Memory within a Virtual Environment

Edgar Chan

An enduring question in research on human navigation is whether memory for object locations in the environment is viewpoint-dependent or viewpoint-independent. One line of research has shown evidence to suggest that cues from the external environment (e.g., room geometry) can play a significant role in how an array of objects is encoded and retrieved. Specifically, retrieval of object-location information tends to be faster and more accurate when the retrieved orientation of the array is aligned with an axis defined by the external cue than when it is misaligned with this axis, even for orientations that were not presented during encoding. My research this year has focused on investigating the role of alignment cues on object-location memory within a novel virtual environment. Typically in my experiments, participants are shown an image of a circular arena containing seven distinct target objects, and are required to learn the locations of the objects to a criterion level of performance. A uniquely coloured square mat placed on the floor of the arena provides the cue to the intrinsic axis of the object array. To test their spatial knowledge of the array, participants are instructed to imagine themselves standing at a particular object location facing another object, and to point to the location of a third object. So far, we have found that participants responded faster and more accurately when the imagined heading was aligned as opposed to misaligned with the axis defined by the mat. We also found that the alignment effect is an enduring property of object-location memory, as it remains evident after a 24 hour delay; and that it can occur in the absence of any external visual cues. The alignment effect remains evident irrespective of whether the encoding of the object locations is achieved through static displays or a process of active navigation. Further studies are being conducted to investigate the influence of visual cueing during retrieval and to explore the neural correlates of the spatial alignment effect using fMRI.

 

Figure 1. Example of the object-array shown to participants during the experiment.

 

 

 

 

 

Publications (2008-2010):

  • Baumann O., Chan E., Mattingley J.B. (2010) Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans. NeuroImage 49:2816-2825  (PDF File 1,035 KB)

Submissions

  • Chan, E., Baumann, O., Bellgrove, M., Mattingley J.B. Reference frames in allocentric representations are invariant over time and encoding perspective (submitted)
  • Chan, E., Baumann, O., Bellgrove, M., Mattingley J.B. Extrinsic reference frames modify the neural substrates of object-location representations (submitted)
  • Chan, E., Baumann, O., Bellgrove, M., Mattingley J.B. Negative emotion during navigation enhances parahippocampal place memory (submitted)
  • Chan, E., Baumann, O., Bellgrove, M., Mattingley J.B. From objects to landmarks: The function of visual information in spatial navigation (submitted)

Conference Abstracts

  • Chan, E., Baumann, O., Mattingley J.B. (2011) Extrinsic reference frames modify the neural encoding of object locations during active spatial navigation. 11th Annual Meeting of the Vision Sciences Society, Naples, USA
  • Baumann, O., Chan, E., Mattingley J.B. (2011) Neural correlates of categorical and coordinate encoding of object locations during active navigation. 11th Annual Meeting of the Vision Sciences Society, Naples, USA
  • Chan, E., Baumann, O., Bellgrove, M., Mattingley, J.B. (2010) The influence of environmental cues on the formation of object-location representations within a virtual environment. 37th Australasian Experimental Psychology Conference, Melbourne, April.
  • Chan, E., Baumann, O., Bellgrove, M., Mattingley, J.B. (2010) The influence of environmental cues on the formation of object-location representations within a virtual environment. 9th Conference of the Australasian Society for Cognitive Science, Sydney, September.
  • Baumann, O., Chan, E., Mattingley, J.B. (2009) Hippocampal, parahippocampal and striatal neuronal activity predicts object-location retrieval during active navigation. 9th Conference of the Australasian Society for Cognitive Science, Sydney, September.
  • Baumann, O., Chan, E., Mattingley, J.B. (2009) Hippocampal, parahippocampal and striatal activity predicts object-location recall during active navigation. Cognitive Neuroscience Society Annual Meeting, San Francisco, USA, March.