2005 Special issueCortico-hippocampal interaction and adaptive stimulus representation: A neurocomputational theory of associative learning and memory
Section snippets
‘Top-down’ model of cortico-hippocampal function in associative learning
What information-processing role does the hippocampus play in classical conditioning? To address this, we developed a computational model of cortico-hippocampal interaction based on connectionist theories of learning and representation (Gluck and Myers, 1993, Gluck and Myers, 1995, Gluck and Myers, 1996, Gluck and Myers, 2001). The model conceptualizes the brain as a series of interacting modules, each implementing the information-processing functions subserved by a particular brain region.
For
Applications to memory disorders in humans
Learned irrelevance is a conditioning phenomenon, in which prior uncorrelated exposure to the CS and US slows subsequent learning of the CS–US association (Mackintosh, 1973). It is similar to the more well-known latent inhibition paradigm (Lubow, 1973), in which an animal is pre-exposed to CS alone trials (rather than uncorrelated CS and US trials as in learned irrelevance), in that both produce slower learning of a subsequence CS–US association. One novel prediction of our cortico-hippocampal
Converging evidence from functional brain imaging in humans
Another method for testing predictions of the model for human learning is functional brain imaging. In particular, our model expects that the medial temporal lobes should be very active early in training when subjects are learning about stimulus–stimulus regularities and evolving a new stimulus representation, but less active later in training when other brain regions (e.g. the basal ganglia) are using these representations to perform the task. In a functional neuroimaging study (Poldrack,
Biological substrates of representational processing in the hippocampal region
While the original cortico-hippocampal model (Gluck and Myers, 1993, Gluck and Myers, 2001) had considerable success at accounting for behaviors of intact and hippocampal-lesioned animals and humans, it has several limitations. The first and most obvious is that it treats the entire hippocampal region as a single functional unit. We describe below how aspects of the earlier model have been mapped onto more physiological mechanisms.
Learning rates and septo-hippocampal cholinergic modulation
The medial septum/diagonal band complex, a structure lying in the basal forebrain, provides important cholinergic inputs to the hippocampus. Physiological studies and prior computational models by Michael Hasselmo suggest that this septo-hippocampal cholinergic input can modulate whether the hippocampus is acting primarily to store new, incoming information, or to retrieve previously-stored information (Hasselmo, 1999, Hasselmo and Schnell, 1994, Meeter et al., 2004). Further, the hippocampus
Redundancy compression and the entorhinal cortex
The hippocampal region is comprised of several distinct and interacting units, including the hippocampus proper (subfields CA1 and CA3), the dentate gyrus, the entorhinal cortex, and the subiculum (Fig. 6). Each of these areas has unique anatomical and physiological characteristics, and each may be expected to provide a unique information-processing function that contributes to the workings of the hippocampal region as a whole.
The entorhinal cortex is the primary path by which sensory
General discussion and future directions
Our general approach has been to work ‘top-down’, starting with connectionist network models that instantiate information-processing theories of the computations required to explain behavior, and then showing how these functions could arise ‘bottom-up’ from the anatomy and physiology of specific brain regions. In this way, computational models can help to elucidate the principles of learning and memory at multiple levels of analysis, from behavioral processes through neural circuits.
There are
Future aims to enhance biological depth
Although we have made some progress at replacing components of our original Gluck and Myers (1993) ‘top-down’ model with biologically-plausible components, much still remains to be done. As described above, we have argued that certain features of our earlier theory of hippocampal-region function can be mapped to specific brain substrates: redundancy compression to the entorhinal cortex and learning rate modulation to septo-hippocampal feedback loops. Several important future aims for
Future aims to enhance behavioral breadth
To date, most of our computational modeling has focused on a relatively constrained area of learning: simple conditioning and those behaviors (like human category learning) that can be understood in terms of conditioning (Gluck & Bower, 1988). However, the hippocampus and associated structures play clear and important roles in other domains, including (but not limited to) declarative learning (Squire, 1987), temporal learning (Levy, 1989) and spatial learning (O'Keefe & Nadel, 1978). Several
Conclusion
A large body of neurobiological and behavioral data on associative learning can be accounted for by assuming that the hippocampal region—including hippocampus proper, entorhinal cortex, and other associated structures—performs an information processing function: compressing (or making more similar) the representations of inputs that co-occur or are otherwise redundant, while differentiating (or making less similar) the representations of inputs that predict different future events. This process
References (90)
- et al.
Neural networks and principal component analysis: Learning from examples without local minima
Neural Networks
(1989) - et al.
A cortical model of winner-take-all competition via lateral inhibition
Neural Networks
(1992) - et al.
Operant behavior suggests attentional gating of dopamine system inputs
Neurocomputing
(2001) - et al.
Activity of dentate granule cells during learning: Differentiation of perforant path input
Brain Research
(1979) - et al.
Early marker for Alzheimer's disease: The atrophic hippocampus
The Lancet
(1989) Complementary roles of basal ganglia and cerebellum in learning and motor control
Current Opinion in Neurobiology
(2000)- et al.
Cerebellar substrates for error-correction in motor-reflex conditioning
Neurobiology of Learning and Memory
(2001) Neuromodulation: Acetylcholine and memory consolidation
Trends in Cognitive Sciences
(1999)- et al.
Free recall and recognition in a network model of the hippocampus: Simulating effects of scopolamine on human memory function
Behavioural Brain Research
(1997) Connectionist learning procedures
Artificial Intelligence
(1989)
Partial quantification of the associative synaptic learning rule of the dentate gyrus
Neuroscience
A computational approach to memory deficits in schizophrenia
Neurocomputing
A computational model of the effects of septohippocampal disruption on classical eyeblink conditioning
Neurobiology of Learning and Memory
Dissociating medial temporal and basal ganglia memory systems with a latent learning task
Neuropsychologia
Memory consolidation, retrograde amnesia and the hippocampal complex
Current Opinion in Neurobiology
Hippocampal and ceocortical contributions to memory: Advances in the complementary learning systems framework
Trends in Cognitive Sciences
Operant behavior during sessions of intravenous cocaine infusion is necessary and sufficient for phasic firing of single nucleus accumbens neurons
Brain Research
A dynamic model of learning in the septo-hippocampal system
Neurocomputing
Differential neuronal encoding of novelty, familiarity, and recency in regions of the anterior temporal lobe
Neuropharmacology
The nature of recollection and familiarity: A review of 30 years of research
Journal of Memory and Language
Selective entorhinal and nonselective cortical–hippocampal region lesions, but not selective hippocampal lesions, disrupt learned irrelevance in rabbit eyeblink conditioning
Cognitive, Affective, and Behavioral Neuroscience
Ibotenic acid lesions of the medial septum retard delay eyeblink conditioning in rabbits (Oryctolagus cuniculus)
Behavioral Neuroscience
Simulation of paleocortex performs hierarchical clustering
Science
Search and decision processes in recognition memory
Temporal sequence compression by an integrate-and-fire model of hippocampal area CA3
Journal of Computational Neuroscience
The restricted influence of sparseness of coding on the capacity of familiarity discrimination networks
Network: Computations in Neural Systems
Comparison of computational models of familiarity discrimination in the perirhinal cortex
Hippocampus
Experience-dependent modifications of hippocampal place cell firing
Hippocampus
How the basal ganglia use parallel excitatory and inhibitory learning pathways to selectively respond to unexpected rewarding cues
The Journal of Neuroscience
Modification of the responses of hippocampal neurons in the monkey during the learning of a conditional spatial response task
Hippocampus
The hippocampal system and declarative memory in animals
Journal of Cognitive Neuroscience
Further studies of hippocampal representation during odor discrimination learning
Behavioral Neuroscience
Intact delay-eyeblink classical conditioning in amnesia
Behavioral Neuroscience
From conditioning to category learning: An adaptive network model
Journal of Experimental Psychology: General
Computational models of the neural bases of learning and memory
Annual Review of Neuroscience
Hippocampal mediation of stimulus representation: A computational theory
Hippocampus
Representation and association in memory: A neurocomputational view of hippocampal function
Current Directions in Psychological Science
Integrating behavioral and physiological models of hippocampal function
Hippocampus
Gateway to memory: An introduction to neural network modeling of the hippocampus in learning and memory
A computational model of the cerebellum and motor-reflex conditioning
Late-training amnesic deficits in probabilistic category learning: A neurocomputational analysis
Learning and Memory
Twenty years of classical conditioning research with the rabbit
Progress in Psychobiology and Physiological Psychology
Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: Computational modeling and brain slice physiology
Journal of Neuroscience
Different ways to cue a coherent system: A theory for episodic, semantic and procedural tasks
Psychological Review
Probabilistic category learning in amnesia
Learning and Memory
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2023, Neuroscience and Biobehavioral ReviewsThe limited role of hippocampal declarative memory in transient semantic activation during online language processing
2021, NeuropsychologiaCitation Excerpt :If true, such an account may predict that individuals with hippocampal damage should retain the ability to map sound to meaning. Furthermore, since the associations have been formed before hippocampal damage, such mappings could well extend to activating related words, i.e., to predictive processing (also see Gluck et al., 2005). On such a view, then, we may expect to see preservation of linguistic prediction in hippocampal amnesia.
Green model to adapt classical conditioning learning in the hippocampus
2020, NeuroscienceRole of hippocampus in polymodal-cue guided tasks in rats
2016, Brain ResearchCitation Excerpt :Nevertheless, the hippocampus is considered a critical brain area where spatial and non-spatial information can be integrated into a unified event representation (Eichenbaum et al., 1999; Moser et al., 2008). Indeed, during new memory formation the hippocampus forms connections between sensory stimuli that can be stored and recalled later (Cohen and Eichenbaum, 1993; Gluck et al., 2005; O’Reilly and Rudy, 2001). To better understand how multiple stimuli combine to produce an appropriate behavior during associative learning, we developed a multisensory apparatus that allows us to measure the navigational behavior along with the precisely controlled presentation of visual, auditory and tactile stimuli.
Computational cognitive models of prefrontal-striatal-hippocampal interactions in Parkinson's disease and schizophrenia
2011, Neural NetworksCitation Excerpt :Similarly, the hippocampus forms recurrent connectivity with various cortical areas, including the prefrontal cortex (Cavada, Llamas, & Reinoso-Suarez, 1983; Goldman-Rakic, Selemon, & Schwartz, 1984; Irle & Markowitsch, 1982; Rosene & Van Hoesen, 1977; Swanson, 1981). As we review below, many computational models focus on simulating the function of the corticostriatal (Frank, 2005; Guthrie, Myers, & Gluck, 2009; Moustafa & Maida, 2007) or corticohippocampal (Gluck & Myers, 1993; Gluck, Myers, & Meeter, 2005; McClelland, McNaughton, & O’Reilly, 1995; O’Reilly & Norman, 2002) connections. Anatomical studies have also identified hippocampal–striatal connections (see for example Shen & Tsai, 1995).
Shared impairment in associative learning in schizophrenia and bipolar disorder
2011, Progress in Neuro-Psychopharmacology and Biological Psychiatry