Neurophysiology of Navigational
Spatial Memory
The place cells of the rodent hippocampus
constitute one of the most striking examples of a correlation
between neuronal activity and complex behavior in mammals.
These cells increase their firing rates when the animal
traverses specific regions of its surroundings, thus
providing a contextually dependent map of the environment.
Because humans rely heavily on visual cues in exploring
their environment, it is unclear whether the place-coding
mechanisms in rodents also are sufficient to characterize
human spatial navigation. Indeed, the human hippocampus
and parahippocampal region receive extensive projections
from visual areas and respond selectively to visual
stimuli. Whereas neuroimaging studies implicate the
hippocampus and paraphippocampal region in human navigation,
the underlying cellular networks remain unknown.
Responses of single neurons were recorded
in six subjects who were patients with pharmacologically
intractable epilepsy undergoing invasive monitoring
with intracranial electrodes to identify seizure focus
for potential surgical treatment. Subjects played a
taxi driver game in which they explored a virtual town,
searching for passengers who appeared in random spatial
locations and delivering them to fixed target locations
(stores).
We directly recorded from 287 neurons
in the temporal and frontal lobes as subjects actively
explored the virtual town. We present evidence for a
neural code of human spatial navigation that includes
cells, primarily in the hippocampus, that respond at
specific spatial locations and celfs, primarily in parahippocampal
region, that respond to views of landmarks. These data
provide a neuroanatomical dissociation between human
hippocampal and parahippocampal function during navigation,
suggesting that the hippocampus is specialized for spatial
position while the parahippocampal region is specialized
for spatial views. Cells throughout the hippocampus,
parahippocampal region, and frontal lobes also responded
to subjects' navigational goals and to conjunctions
of place, goal, and view during our virtual spatial
exploration task.
