Theme 4: From physical to conceptual spaces

Humans are exquisite navigators, yet little is known about the environmental cues upon which we rely when finding our way in new or otherwise unfamiliar environments. Research in this theme has sought to determine the neural and cognitive processes responsible for object location-memory and landmark-based navigation in adult human participants. Across a series of experiments, the team has used functional magnetic resonance imaging to reveal the neural correlates of encoding and retrieval of visual landmarks in novel, virtual arenas. The research has also discovered, for the first time, a dedicated human brain region that encodes heading direction, a cue that is crucial in most way-finding situations. In further experiments, the team has demonstrated that the spatial disposition of contextual cues, such as those relating to the alignment of object locations relative to one another within a novel environment, exerts a unique influence on cognitive and neural representations of visual space. Finally, the team has examined the effects of cerebral stroke on a variety of navigation processes.

 

Project Members

Theme Leader	Jason Mattingley
Chief Investigators	Michael Arbib, John O’Keefe, Andrew Smith, Janet Wiles, Gordon Wyeth
Research Fellow	Oliver Baumann
PhD Student	Edgar Chan
Technology Support and Research Assistants	Jack Valmadre (2010), Daniel Clark (2009), Mark Wakabayashi (2007), Robert Ninnes  and Ashley Skilleter
Collaborators	In Thinking Systems: Paul Stockwell
Honours Student	Amy Collins

Neural and Behavioral 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).

 

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).

 

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).

 

 

 

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).

 

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.

We are currently finalising a series of follow-up studies, with the aim to investigate further aspects of how humans use, process and memorise 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.

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.

Publications (2008-2010):

Baumann, O., Mattingley, J.B. (2010b) Medial parietal cortex encodes perceived heading direction in humans. Journal of Neuroscience 30: 12897-12901.

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.

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.

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.

Baumann, O., Greenlee, M.W. (2009) Effects of attention to auditory motion on cortical activations during smooth pursuit eye tracking. PLoS ONE 4:9

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.

Submissions

Baumann O., Skilleter, A., Mattingley J.B. Short-term Memory Maintenance of Object Locations during Active Navigation: Which Working Memory Subsystem is Essential?

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.

Conference Abstracts

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.

Related Activities

Guest lecture on human spatial navigation in the Cognitive Neuroscience course at the School of Psychology, University of Queensland, Brisbane (2010)

Invited speaker at the QBI Neuroscience Seminar, Brisbane (2010)

Attendee at the Brain Products Workshop and Training Course, Brisbane (2010)

Poster presentation at the Human Brain Mapping Meeting, Barcelona, Spain (2010)

Oral presentation at the 37th Australasian Experimental Psychology Conference, Melbourne (2010)

Invited speaker at the Summer School on Animal Navigation, Brisbane (2009)

Guest lecture on human spatial navigation in the Cognitive Neuroscience course at the School of Psychology, University of Queensland, Brisbane (2009)

Oral presentation at the 9th Conference of the Australasian Society for Cognitive Science, Sydney (2009)

Poster presentation at the Cognitive Neuroscience Society Annual Meeting, San Francisco, USA (2009)

Attendee at the FSL & Freesurfer course, Brisbane (2009)

Guest lecture on human spatial navigation in the Cognitive Neuroscience course at the School of Psychology, University of Queensland, Brisbane (2008)

Poster presentation at the Human Brain Mapping Meeting, Melbourne (2008)

Poster presentation at the Cognitive Neuroscience Society Annual Meeting, San Francisco, USA (2008)

Attendee at the Summer School on Animal Navigation, ANU, Canberra (2007)

Supervision of undergraduate, summer or honours students related to Thinking Systems

Supervision of an Honour’s thesis at the School of Psychology, University of Queensland: Working Memory in Spatial Navigation: Which Subsystem is Essential for Object Location Memory?  Amy Collins, BSc (2009)

Grants

Baumann, O., Mattingley, J.B. UQ New Staff Start-up Grant: Topographic and temporal analysis of cerebellar neural activity related to attentional, perceptual and memory processes (2008).

Mattingley, J.B., Greenlee, M.W., Baumann, O.B. Go8 Germany Joint Research Co-operation Grant:  Visual-Vestibular Interactions for active navigation and spatial object-location memory (2010-2011).

Media Coverage

O. Baumann. Australian Geographic: “Sense of direction can be learned” (08.10.2010)  http://www.australiangeographic.com.au/journal/sense-of-direction-can-be-learned.htm

O. Baumann. Queensland Brain Institute scientists find the brain's inner compass. Courier Mail.  http://www.couriermail.com.au/news/queensland/queensland-brain-institute-scientists-find-the-brains-inner-compass/story-e6freoof-1225931978553

O. Baumann. ABC Online: “Study locates our sense of direction” (30.09.2010)
http://www.abc.net.au/science/articles/2010/09/30/3025268.htm

O. Baumann. CBC Online: “Brain’s sense of direction located” (30.09.2010)
http://www.cbc.ca/technology/story/2010/09/30/direction-brain.html

O. Baumann. Daily News and Analysis: “How our brains ‘light up’ when we navigate” (30.09.2010)
http://www.dnaindia.com/scitech/report_how-our-brains-light-up-when-we-navigate_1445632

O. Baumann. Courier Mail: “Magnetic personality or not, we all have an inner campus” (30.09.2010)

O. Baumann. Sydney Morning Herald: “Mapping the brain” (30.09.2010)

O. Baumann. 702 ABC Sydney Radio Interview (30.09.2010)

O. Baumann. 91.7 ABC Coast FM Radio Interview (30.09.2010)

O. Baumann. Sydney Morning Herald: “Mapping the brain” (30.09.2010)

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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.

 

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