Although the mammalian basal ganglia have long been implicated in motor behavior, it is generally recognized that the behavioral functions of this subcortical group of structures are not exclusively motoric in nature. Extensive evidence now indicates a role for the basal ganglia, in particular the dorsal striatum, in learning and memory. One prominent hypothesis is that this brain region mediates a form of learning in which stimulus-response (S-R) associations or habits are incrementally acquired. Support for this hypothesis is provided by numerous neurobehavioral studies in different mammalian species, including rats, monkeys, and humans. In rats and monkeys, localized brain lesion and pharmacological approaches have been used to examine the role of the basal ganglia in S-R learning. In humans, study of patients with neurodegenerative diseases that compromise the basal ganglia, as well as research using brain neuroimaging techniques, also provide evidence of a role for the basal ganglia in habit learning. Several of these studies have dissociated the role of the basal ganglia in S-R learning from those of a cognitive or declarative medial temporal lobe memory system that includes the hippocampus as a primary component. Evidence suggests that during learning, basal ganglia and medial temporal lobe memory systems are activated simultaneously and that in some learning situations competitive interference exists between these two systems.
The present experiments were designed to examine the hypothesis that the mammalian brain contains anatomically distinct memory systems. Rats with bilateral lesions of caudate nucleus or fimbria-fornix and a control group were tested postoperatively on 1 of 2 versions of the radial maze task. In a standard win-shift version, each of the 8 arms of the maze was baited once, and the number of errors (revisits) in the first 8 choices of each trial was recorded. Fimbria-fornix rats were impaired in choice accuracy, while caudate animals were unimpaired relative to controls. Different groups of rats with similar lesions were tested on a newly developed win-stay version of the radial maze, in which the location of 4 randomly selected baited arms was signaled by a light at the entrance to each arm, and which required rats to revisit arms in which reinforcement had been previously acquired within a trial. Rats with fimbria-fornix lesions were superior to controls in choice accuracy on the win-stay radial maze task, while caudate animals were impaired relative to controls. The results demonstrate a double dissociation of the mnemonic functions of the hippocampus and caudate nucleus. Some implications of the presence of 2 memory systems in the mammalian brain are discussed.
The present study examined the effect of lesions of the caudate nucleus or fimbria-fornix on the acquisition of two water maze tasks. In both tasks, two rubber balls with different visual patterns were used as platforms (i.e., cues). The "correct" cue was attached to a submerged rectangular platform and could be mounted by an animal to escape the water. The "incorrect" cue was attached to a thin round pedestal and could not be mounted. In a spatial version of the task, the correct cue was located in the same quadrant of the maze on all trials, whereas the visual pattern on the cue was varied from trial to trial. Lesions of the fornix, but not the caudate nucleus, impaired acquisition of this spatial task in relation to control animals. In a simultaneous visual discrimination version of the task, the correct cue on all trials was one with a specific visual pattern, and the spatial location of the correct cue was varied from trial to trial. Lesions of the caudate nucleus, but not the fornix, impaired acquisition of this visual discrimination task in relation to control animals. The double dissociation observed supports the hypothesis that the hippocampus and caudate nucleus are parts of systems that differ in the type of memory they mediate.
These experiments investigated the effects, on memory, of injections of d-amphetamine (10 pg/0.5 id) adminitered into the amygdala, hippocampus, or caudate nucleus immediately after traning in cued or spatial water-maze tasks. In experiment 1, rats received an eight-trial training session on one of the two tasks followed by injections of d-amphetamlne or saline. The amygdala is known to project to both the hippocampus and caudate nucleus (17)(18)(19)(20), and the finding that c-fos is expressed in hippocampus and caudate nucleus following intraamygdala injections of the excitatory amino acid N-methyl-D-aspartate (21) indicates that the amygdala is functionally connected with both of these structures. Such evidence suggests the possibility that the amygdala may influence both hippocampal-and caudate-dependent memory.To investigate this implication, experiment 1 examined the effects of posttraining intraamygdala injections of d-amphetamine on memory for two different types of water-maze tasks-a spatial task and a cued task-that are known to differentially involve the hippocampus and caudate nucleus, respectively (4, 22, 23). d-Amphetamine was used in these experiments because of extensive evidence that d-amphetamine enhances retention of a variety of tasks when administered either centrally (5, 24) or peripherally (25,26).In the spatial task, rats were trained to swim to an escape platform placed in a constant spatial location. As the top of the platform was 1.0 cm below the water surface, and rats were trained to approach the platform from different start points, the platform could be located only by learning spatial relationships among distal extramaze cues. In the cued task, rats were trained to swim to a visible cue mounted on a platform, which was placed in a different spatial location on each trial.Experiment 2 was designed to determine whether the amygdala was involved as a locus of changes mediating the amygdala influences on memory in these two tasks. Rats were trained on one of the two tasks, given posttraining intraamygdala injections of d-amphetamine or saline, and then, shortly before testing, given an intraamygdala injection of lidocaine to inactivate the amygdala. Apparatus. The water maze was a black circular galvanized steel tank (diameter, 1.83 m; height, 0.58 m) filled with water (250C) to a depth of 20 cm. Four starting positions (north, south, east, west) were equally spaced around the perimeter of the tank, dividing the pool into quadrants. The rectangular Plexiglas escape platform used for the spatial task (11 x 14 x 19 cm) was submerged at a depth of 1 cm. For the cued task, a black and white striped rubber ball (diameter, 8 cm) was attached to the top of the submerged platform and protruded above the water surface. The platform could be used as a step to mount the ball and escape the water. MATERIALS AND METHODSSurgery. Animals were anesthetized with sodium pentobarbital (50 mg/kg). Unilateral guide cannulae were implanted on the left side by standard stereotaxic techniques. For th...
Stress is a biologically significant factor shown to influence synaptic plasticity and memory functioning in the hippocampus. This study examined the role of the amygdala, a brain structure implicated in coordinating stress behaviors and modulating memory consolidation, in mediating stress effects on hippocampal long-term potentiation (LTP) and memory in rats. Electrolytic lesions of the amygdala effectively blocked the adverse physiological and behavioral effects of restraint and tailshock stress, without impeding the increase in corticosterone secretion to stress. Physiologically, hippocampal slices from stressed animals exhibited impaired LTP relative to slices from unstressed control animals, whereas hippocampal slices from stressed animals with amygdalar lesions exhibited normal LTP. Behaviorally, stressed animals were impaired in retention of a hippocampal-dependent hidden platform version of the Morris water maze task, and this impairment was blocked by amygdalar lesions. In a fixed location-visible platform water maze task that can be acquired by independent hippocampal and nonhippocampal memory systems, stress enhanced the use of nonhippocampal-based memory to acquire the task. These results indicate that an intact amygdala is necessary for the expression of the modulatory effects of stress on hippocampal LTP and memory.
A cross-maze task that can be acquired through either place or response learning was used to examine the hypothesis that posttraining neurochemical manipulation of the hippocampus or caudate-putamen can bias an animal toward the use of a specific memory system. Male Long-Evans rats received four trials per day for 7 days, a probe trial on day 8, further training on days 9 -15, and an additional probe trial on day 16. Training occurred in a crossmaze task in which rats started from a consistent start-box (south), and obtained food from a consistent goal-arm (west). On days 4 -6 of training, rats received posttraining intrahippocampal (1 g͞0.5 l) or intracaudate (2 g͞0.5 l) injections of either glutamate or saline (0.5 l). On days 8 and 16, a probe trial was given in which rats were placed in a novel start-box (north). Rats selecting the west goal-arm were designated ''place'' learners, and those selecting the east goal-arm were designated ''response'' learners. Saline-treated rats predominantly displayed place learning on day 8 and response learning on day 16, indicating a shift in control of learned behavior with extended training. Rats receiving intrahippocampal injections of glutamate predominantly displayed place learning on days 8 and 16, indicating that manipulation of the hippocampus produced a blockade of the shift to response learning. Rats receiving intracaudate injections of glutamate displayed response learning on days 8 and 16, indicating an accelerated shift to response learning. The findings suggest that posttraining intracerebral glutamate infusions can (i) modulate the distinct memory processes mediated by the hippocampus and caudate-putamen and (ii) bias the brain toward the use of a specific memory system to control learned behavior and thereby influence the timing of the switch from the use of cognitive memory to habit learning to guide behavior. A ccording to the ''multiple memory systems'' hypothesis, different forms of memory are organized in independent brain systems. This hypothesis is supported by studies involving several mammalian species, including rats (1-6), monkeys (7-10), and humans (11)(12)(13)(14). For example, in rats, findings from double-dissociation experiments using lesion (3-6, 15) and posttraining intracerebral drug injection techniques (16)(17)(18)(19) indicate that the hippocampal system and caudate-putamen are parts of independent memory systems.Characteristics of the psychological operating principles that distinguish multiple memory systems have been proposed by numerous investigators (e.g., refs. 1, 2, 8, 9, 11, 13, 20, and 21), and the design of each of these theories, particularly those derived from animal research, has been influenced to some extent by the historical debate between ''cognitive'' and ''stimulus-response'' (S-R) animal learning theorists. The cognitive view, exemplified by the early work of Tolman (22,23), holds that animals acquire knowledge-based expectations that serve to guide behavior in a purposeful manner, a form of learning in which relatio...
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