As mammals repeatedly experience sensory events, neurons in their sensory cortices gradually become tuned to specific features of those events. Might similar processes explain the kinds of latent learning observed when individuals actively explore the world around them? Researchers have attempted to answer this question by measuring and manipulating brain activity in rodents perform-ing spatial tasks. Initially, the emphasis was on discoverperform-ing where memories of mazes were stored in the cortex. Karl Lashley’s failed attempt to locate cortical engrams for maze learning in rats (described in Chapter 2) represents one of the
earliest attempts. Later neurophysiological studies of rats navigating through mazes revealed that spatial learning actually depends much more on activity in the hippocampus than on cortical engrams.
The hippocampus is one of the most extensively studied brain regions in the field of learning and memory. In humans and other primates, the hippocampus is a relatively small structure lying just beneath each temporal lobe (see Figure 2.3 and Figure 3.16a). In rodents, however, the hippocampus makes up a much larger proportion of the brain (Figure 3.16b). Many other vertebrates, includ-ing birds and reptiles, also possess a hippocampus. Although the hippocampus in birds is proportionately smaller than in rodents (Figure 3.16c), the absolute size of a bird’s hippocampus is known to be important for spatial memory.
Specifically, birds storing their food in many different locations for use in the winter have a hippocampus that is bigger than in related bird species that do not need to keep track of hidden food (Sherry & Hoshooley, 2010). Generalizing across species, you might expect that given the size of their hippocampus, rats should be quite adept at spatial learning. This prediction is borne out by the success with which rats learned to traverse thousands of different mazes during the early history of psychological research.
Identifying Places
As a first step toward understanding the role of the hippocampus in spatial learning, English neuroscientist John O’Keefe implanted electrodes in rats’ hip-pocampal regions to record neuronal activity under various conditions (O’Keefe
& Dostrovsky, 1971). When the rats were placed in an environment and allowed to explore freely, the investigators made a surprising discovery. Some hippocam-pal neurons seemed to fire only when a rat wandered into particular locations, and other hippocampal neurons fired only when the rat was in other locations.
O’Keefe coined the term place cells to refer to neurons with such spatially tuned firing patterns. Each of these neurons had a certain preferred location to which it responded with maximal activity, and this location was termed the place field for that neuron (analogous to the receptive fields of sensory corti-cal neurons described above). The activity of these cells was so reliable that a blindfolded researcher could tell when a rat entered a particular region of the maze just by hearing the corresponding place cell begin to fire. O’Keefe sug-gested that place cells might form the basis for spatial learning and navigation.
How might place cells help with spatial navigation? If a certain neuron fires only when an individual is in a particular place, then that neuron might serve as an identifier for that place (much like road signs at street corners or mile mark-ers along the highway). When the neuron fires, the brain would then “know”
that the body is in a particular location. If you had enough place cells to code for every possible location you’ve ever visited—or ever might visit—you could work out where you are just by noting which place cell is firing. Of course, that would
Hippocampus within medial temporal lobes
(a) Monkey
Hippocampus (b) Rat
Hippocampus (c) Bird
Figure 3.16 The hippocampus in several types of animals Cross sections showing the hippocampus in a monkey, rat, and bird.
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109require an incredibly large number of place cells. Such a method, in which cells are kept on reserve to encode locations that you haven’t yet visited, would be extremely wasteful. Instead, it would be smarter to create place cells as you need them. In other words, place fields should form during learning, as an animal explores its environment. This turns out to be the case.
An explanation of how place cells work must begin with a discussion of what defines a place. Put another way, what exactly determines whether a place cell will respond? Part of what leads a place cell to respond seems to be the animal’s inner sense of its location in space: a rat’s place cells often continue to respond in an orderly fashion even when the rat is running through a maze with the lights out. But place cell responses also depend heavily on visual inputs. For example, suppose a rat is allowed to explore a maze like the one shown in Figure 3.17a.
This maze has three identical arms (labeled 1, 2, and 3 in the figure) differenti-ated by one salient visual cue: a card placed outside the maze between arms 2 and 3. After the initial exploration, various place cells in the rat’s hippocampus will have place fields corresponding to parts of this maze. One hippocampal neuron, for example, had the place field shown in Figure 3.17b (darker areas indicate maximal firing; lighter areas, lesser firing). In other words, this place cell responded preferentially when the rat was in the southwest corner of the maze (as oriented in Figure 3.17a), at the outer edge of arm 2, on the side near-est the card (Lenck-Santini, Save, & Poucet, 2001).
Now suppose the experimenter takes the rat out of the maze and rotates the maze and card 120 degrees clockwise. What do you think will happen when the rat is put back in the maze (Figure 3.17c)? Will the place cell continue to fire when the rat is in the southwest corner of the maze? Or will it fire when the rat is at the end of arm 2, even though that is now the north-most corner of the maze? The answer is shown in Figure 3.17d: the place cell’s preferred location has rotated along with the maze. In this particular case, since the three arms all look, smell, and feel pretty similar, the rat probably used the visual cue as a landmark. When the maze was rotated again, another 120 degrees clockwise, but the card was returned to its original place (Figure 3.17e), then the place
(a)
Figure 3.17 Effects of a visual landmark on a rat’s place field Upper images show the rat’s environment: a three-armed maze and a visual cue (a card, location marked in dark purple). Lower images show how a representative place cell fires in this environment: dark areas are regions that evoke heavy firing;
lighter areas, regions that evoke lesser firing. (a, b) When the maze is in its initial position, this place cell fires maximally when the rat is in arm 2. (c, d) When maze and cue card are rotated 120 degrees clockwise, the place field is deter-mined by visual cues; maximal firing still occurs in arm 2. (e, f) If the maze is rotated another 120 degrees but the card is returned to its original location, the place cell fires when the rat is in the south-west corner, even though this is now arm 3. In other words, place cell firing seems to depend on the rat’s estimation of its location based on the visual landmark.
(Adapted from Lenck-Santini et al., 2001.)
cell again fired in the southwest corner of the maze, even though this was now arm 3 (Figure 3.17f). These findings illustrate the importance of visual land-marks (such as the card) in determining when a hippocampal place cell will fire.
In addition to landmarks, some place cells in rats seem to be sensitive to other variables, such as the speed or direction in which a rat is moving. Thus, place cells respond like sensory cortical neurons with multimodal receptive fields.
Some place cells have place fields that are stable for months: if the rat is returned to the maze in Figure 3.17 after a long absence, the same place cell may still fire when the rat is in the same location as before. Research also shows that when place fields are unstable, spatial navigation is disrupted. The stability of place fields and their selectivity in terms of particular visual scenes are consistent with the idea that place cells provide the basis for a “cognitive map” that rats use to navigate through the world. But how, exactly, do place cells become tuned to a particular place?
One factor affecting the creation of place fields is experience. When rats repeatedly experience an environment, their place cells become increasingly tuned to locations within that environment (Lever, Wills, Cacucci, Burgess, &
O’Keefe, 2002). Imagine the size of the dark place field in Figure 3.17 (b, d, and f) getting smaller and smaller, providing an increasingly precise and reli-able report of where in the maze the rat is. This place-field shrinkage seems to correlate with rats’ spatial navigation abilities in a maze; experiments in which rats’ place-field shrinkage is disrupted (for example, by blocking inputs from the thalamus) show that the rats’ spatial learning abilities decline (Cooper &
Mizumori, 2001; Mizumori, Miya, & Ward, 1994; Rotenberg, Abel, Hawkins, Kandel, & Muller, 2000).
The findings presented above suggest that spatial learning that occurs during exploration is correlated with changes in the stability and selectivity of place cells (Rosenzweig, Redish, McNaughton, & Barnes, 2003). This phenomenon may explain how Tolman’s rats were able to latently learn the layout of a com-plex maze even without associating specific locations with food rewards. Perhaps as the nonrewarded rats explored the maze, their place fields shrunk as much as (or more than) those of the rewarded rats, providing them with a precise representation of various locations within the maze that they could later take advantage of when the researchers initiated training with food.
Recognizing Objects
In order to use visual landmarks to navigate within a maze, rats must be able to recognize those landmarks. This suggests that as rats explore an environment, they not only learn how to navigate through that environment, but they also learn the properties of objects within and around the paths they are traveling.
Recall that some of the earliest evidence of visual perceptual learning came from studies in which triangles and circles were mounted in the home cages of rats. If hippocampal neurons are sensitive to visual landmarks within a maze, might they also contribute to a rat’s ability to recognize and distinguish those landmarks?
Recent studies have examined this possibility in rats performing the novel object recognition task described earlier. In initial experiments, researchers lesioned the hippocampus of rats after the rats had repeated experiences explor-ing fixed configurations of objects. Rats with hippocampal damage showed impaired object recognition memory, exploring objects that they had experi-enced many times as if they had not seen them before. Later studies found, however, that such lesions disrupted object recognition in certain situations only (Langston & Wood, 2010)—specifically, those in which memories of the posi-tion of the object and the context in which it was experienced were integrated.
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111These findings suggest that hippocampal neurons contribute to exploratory learning in ways that go beyond simply constructing spatial maps or identifying familiar objects. As you study further in this book, you will discover many more ways that the hippocampus and surrounding regions contribute to learning and memory.
Interim Summary
■ In Aplysia, habituation is the result of synaptic depression in circuits that link sensory neurons to motor neurons. In contrast, sensitization in Aplysia reflects increases in synaptic transmission caused by the activation of interneurons.
■ During perceptual learning, cortical neurons refine their responses to sen-sory inputs as discrimination abilities improve.
■ In Hebbian learning, repeated exposures can strengthen associations between particular subsets of cortical neurons, causing neurons that fire together to wire together. This process can increase the ability to recognize repeated stimuli.
■ Hippocampal place cells are neurons that become most active when an animal is at a particular location. These neurons may help animals identify and navigate through familiar environments.
3.3 Clinical Perspectives
Even when you are not consciously aware of it, perceptual learning influences every experience you have. From your ability to understand speech to your ability to find your way to school or work, every sensation and perception is influenced by the memories you’ve acquired through repeatedly experiencing similar stimuli. As noted earlier in this chapter, much of perceptual learn-ing involves processlearn-ing in sensory cortices. The cortical regions that process sensory information can be damaged through brain injury, and the result can be a fundamental change in how stimuli are perceived, processed, and learned about, which in turn will affect processes of habituation, perceptual learning, and familiarization.