spatial navigation

Neural basis of spatial navigation in the congenitally blind

neurophilosophy — Wed, 30 Jun 2010 13:55:25 +0000

Neural basis of spatial navigation in the congenitally blind

FOR most of us, the ability to navigate our environment is largely dependent on the sense of vision. We use visual information to note the location of landmarks, and to identify and negotiate obstacles. These visual cues also enable us to keep track of our movements, by monitoring how our position changes relative to landmarks and, when possible, our starting point and final destination. All of this information is combined to generate a cognitive map of the surroundings, on which successful navigation of that environment later on depends.

Despite the importance of vision for navigation, congenitally blind people - those born blind - can still generate neural representations of space. Exactly how is unclear, but it is thought to be by using a combination of touch, hearing and smell, and some are even known to use echolocation. Spatial navigation in the congenitally blind is therefore thought to involve different brain networks than those engaged in sighted people. A team of Danish researchers now report, however, that the mechanisms underlying spatial navigation in the blind are much the same as those in sighted people, due to the brain's remarkable ability to reconfigure itself.

The new study, by Ron Kupers and Daniel-Robert Chebat, involved two separate experiments using the same navigation task. In the first, 10 congenitally blind and 10 blindfolded sighted participants spent 4 days learning a route navigation and route recognition task using the BrainPort tongue-display unit (below), a sensory substitution device which translates visual images into touch sensations applied to the tongue.

The principle of sensory substitution was established in the 1960s by Paul Bach-y-Rita, who demonstrated it with a "tactile-vision" device consisting of an old dentist's chair with hundreds of vibrating solenoid stimulators incorporated into the back rest. These acted a bit like pixels, generating a tactile representation of images from a television camera, which was accurate enough to enable blind people to discriminate between objects. This is possible because of the brain's ability to re-route sensory information along novel pathways, one form of the phenomenon referred to as neuroplasticity.

In the navigation task, the participants learned to navigate their way through two virtual routes (above) presented onto their tongues by the device, using the arrow keys on a computer keyboard. At the end of each training day, they were asked to draw each of the virtual routes, to verify that they had generated a cognitive map. In the route recognition task, the participants were automatically guided through the routes by the computer program, and then had to indicate which of the routes had been presented to them by means of the tongue-display unit. Overall, there was no difference in performance between the two groups - both the blind and the sighted participants successfully learned both of the routes, and their drawings became increasingly accurate after each training day.

When, however, they repeated the route recognition task while lying in a brain scanner, important differences in the brain activation patterns were observed. In the blind participants, route recognition produced strong activation of several distinct sub-regions of the visual cortex, and of the right parahippocampus, which is known to contain cells that are involved in spatial navigation. In contrast, the sighted participants exhibited no increase whatsoever in visual cortical or parahippocampal activity. Instead, the task led to activation of various frontal cortical areas. In the second experiment, 10 more sighted participants were trained to perform the same route recognition without blindfolds. They didn't use the tongue display unit either - the virtual routes were presented to them on a computer screen instead. When they repeated it in the brain scanner, the brain activation pattern observed was very similar to that seen in the blind participants in the first experiment.

Although there are numerous studies of how the brain is reorganized following sensory loss, this is one of only a small handful that use functional neuroimaging to investigate the neural basis of spatial navigation in the congenitally blind. One interesting finding is that the hippocampus itself, which is known to contain at least four cell types involved in spatial navigation, was not activated in any of the participants. This may be because it is more important for encoding of cognitive maps, but not their subsequent retrieval. The participants spent 4 days learning the routes, by which time their maps were likely encoded strongly. There is also some evidence that the hippocampus encodes spatial information related to external cues, whereas the parahippocampus encodes it in relation to one's own movements. The frontal cortical activation observed in the sighted participants suggest that they may use a different navigational strategy, one that involves decision-making.

Because of the limited resolution of the tongue display unit, the routes used in the navigation tasks were simplifed versions of computerized mazes that lacked usual environmental features such as landmarks. It is possible, therefore, that the tasks were not demanding enough, but solving them did involve generating cognitive maps, and they were made harder because the sensory information was tactile rather than visual. The study therefore provides evidence that spatial navigation in the absence of vision depends upon the parahippocampus and visual cortex. The findings also suggest that cognitive maps can develop in the complete absence of visual experience, because the visual cortex is capable of processing spatial information received by non-visual senses such as touch.

Related:

Kupers, R. et al. (2010). Neural correlates of virtual route recognition in congenital blindness Proc. Nat. Acad. Sci. DOI: 10.1073/pnas.1006199107.

Bach-y-Rita, P. W. & Kercel, S. (2003) Sensory substitution and the human-machine interface. Trends. Cogn. Sci. 7: 541-546. [PDF]

neurophilosophy Wed, 06/30/2010 - 09:55

Human grid cells tile the environment

neurophilosophy — Wed, 27 Jan 2010 11:40:04 +0000

Human grid cells tile the environment

HOW does the brain encode the spatial representations which enable us to successfully navigate our environment? Four decades of research has identified four cell types in the brains of mice and rats which are known to be involved in these processes: place cells, grid cells, head direction cells and, most recently, border cells. Although the functions of most of these cell types are well characterized in rodents, it remains unclear whether they are also found in humans. A new functional neuroimaging study, by researchers from University College London, published online in the journal Nature, now provides the first evidence for the existence of grid cells in the human brain.

Grid cells were discovered in 2005 by Edvard and May-Britt Moser of the Kavli Institute for Systems Neuroscience in Trondheim, Norway, using multi-electrode arrays chronically implanted into the hippocampus and surrounding regions of freely moving mice. Whereas place cells fire when the animal is in a unique, specified position in its environment, grid cells - which are located in the entorhinal cortex - increase their activity in multiple locations, firing periodically as the mouse traverses a space. When a grid cell's activity is correlated with the animal's position and trajectory, and then superimposed onto a map of the environment, it is found to define a repeating pattern of equilateral triangles which 'tiles' the space (panel b, below). Each cell is activated whenever the animal's position coincides with any vertex in this grid, but each has its own periodicity, and so 'tiles' the environment using a unique scale.

Christian Doeller of UCL's Institute of Cognitive Neuroscience and his colleagues first carried out a series of experiments in which grid cell activity was recorded from the brains of mice. This revealed several previously unknown properties of the cells. First, they found that grid cell activity is modulated by the direction in which the animals are moving, so that the increase in grid cell activity is greater when the animals move along the main axes of the grids. Further, they found that the activity of the cells is also modulated by running speed - the faster the animals moved, the more the quickly they crossed the virtual triangle boundaries encoded by the grid cells and, as a result, the shorter was the interval between each burst of activity.

The researchers reasoned that if grid cells exist in the human brain, the activity of the population as a whole should produce a signal that is large enough to be detected by functional neuroimaging. And, because the orientations of the triangular grids encoded by the cells in the population are all aligned to each other, the activation pattern should exhibit six-fold rotational symmetry. They therefore recruited 42 male participants, and scanned their brains while they explored a circular virtual reality environment consisting of a grassy plain bounded by a cliff and surrounded by mountains (panel a, below).

When they analyzed the fMRI data, the researchers found that the signal was modulated by direction and running speed, just as they had predicted. The grid orientation appeared to vary randomly between the participants, suggesting that the activity of grid cells is independent of landmarks in the surroundings. In each participant, however, the increase in entorhinal cortex activity was greatest when their movements through the virtual environment were aligned with the three main grid axes. That is, the signal exhibited 6-fold rotational symmetry; no activity with 4-, 5-, 7- or 8-fold symmetry was observed. The signal obtained during high speed movements was also stronger than the one recorded during slower movements (panels c and d, above).

While navigating the virtual environment, the participants were required to collect various objects and then return them to the same location. In their analyses, the researchers also found that the signal obtained was related to performance on this memory task - the more coherent the signal, the better was the participant's performance. The regions from which neuronal activity was recorded overlaps extensively with brain areas known to be involved in encoding and retrieval of autobiographical memory. This provides some insight into the neural basis of this type of memory; it suggests that the brain may use information about both time and space when encoding life events.

Unlike most functional neuroimaging studies, which simply correlate behaviours with patterns of brain activation, this one is driven is hypothesis. The researchers made predictions about the signal they would expect to see, based on known properties of grid cell activity. They only provide indirect evidence that grid cells exist in the human brain, however. Obtaining solid evidence would involve implanting electrodes into the brain, which is unfeasible in healthy participants. Epileptic patients undergoing pre-surgical evaluation afford a unique opportunity to investigate neuronal function directly; perhaps researchers will try to investigate the cellular basis of spatial navigation in this situation.

Nevertheless, this study suggests that the human brain, like that of mice and rats, uses a regularly repeating grid-like geometry to encode representations of space. The hippocampus and surrounding areas are known to be the first to degenerate in Alzheimer's Disease, so the findings present may also help to explain why disorientation is one of the first behavioural manifestations of the condition.

Related:

Doeller, C., et al. (2010). Evidence for grid cells in a human memory network Nature DOI: 10.1038/nature08704.

neurophilosophy Wed, 01/27/2010 - 06:40

Mice navigate a virtual reality environment

neurophilosophy — Sun, 18 Oct 2009 17:30:38 +0000

Mice navigate a virtual reality environment

USING an inventive new method in which mice run through a virtual reality environment based on the video game Quake, researchers from Princeton University have made the first direct measurements of the cellular activity associated with spatial navigation. The method will allow for investigations of the neural circuitry underlying navigation, and should lead to a better understanding of how spatial information is encoded at the cellular level.

In mice, spatial navigation involves at least four different cell types located in the hippocampus and surrounding regions. Place cells increase their activity when the animal is in a specific location within its environment, called the place field. Grid cells, by contrast, fire periodically as the animal traverses a space; each has a unique periodicity, and apparently measures out the space using its own scale. Head direction cells, as their name implies, fire when the animal is facing a particular direction and border cells, which were identified only last year, encode the animal's distance from the borders within its environment.

Place cells were discovered almost 40 years ago and are the most extensively studied of these cell types. Their activity is typically recorded using small arrays of microelectrodes implanted within the hippocampus of a freely moving rodent. The arrays can remain in place for days or weeks, during which time they can be used to monitor changes in place cell firing rates, and how the acitivty of cells is related to the animal's movements within its environment. They record from afar, because the animal's movements prevent them from coming into, and maintaining, close contact with the cells.

In the ingenious set-up devised by members of David Tank's laboratory, the mice were restrained, and ran on a spherical treadmill supported by a jet of air. Information about the rotation of the treadmill was used to control the animals' movements along a computer-generated track which was projected onto a surrounding screen.

In this virtual environment, the place cells behaved as expected. All the cells from which recordings were made generated short, regular bursts of nervous impulses, separated by intervals of about one tenth of a second,. This produced a low level of background activity called the theta oscillation, which has a frequency of 6-10 cycles per second, and which is characteristic of the hippocampus. The actvity of individual place cells was modulated by location. As the animal entered a given place field, the corresponding place cell increased its firing rate almost five-fold, to generate a rhythmic discharge with a higher frequency than the background.

Because the animals were stationary, the electrodes could be used to record directly from the place cells, enabling the researchers to measure their dynamical electrical properties. This revealed how their firing rate increases: as the mouse approached a place field, the corresponding cell would ramp up its resting membrane voltage. This would cause the cell to increase the frequency of its impulses while the mouse ran through the field. When the animal emerged from the other side of the field, the membrane voltage would go back down to its normal level, and the frequency of impulses would decrease again. The background activity of single cells was also found to increase while the animal was in the appropriate location.

These findings are consistent with the predictions of a model which states that place cell activity is modulated by interactions between two separate oscillating inputs. The data do not exclude other possibilities, however, and the availablity of this virtual reality system will enable researchers to study the activity of place cells in greater detail, because it offers researchers the ability to design highly customized environments, and can be used in combination with other techniques such as two-photon laser scanning microscopy.

Related:

Harvey, C., et al. (2009). Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461: 941-946. DOI: 10.1038/nature08499.

neurophilosophy Sun, 10/18/2009 - 13:30