Thomas T. Hills

Dopamine and Glutamate Control Area-Restricted Search Behavior in Caenorhabditis elegans

Area-restricted search (ARS) is a foraging strategy used by many animals to locate resources. The behavior is characterized by a time-dependent reduction in turning frequency after the last resource encounter. This maximizes the time spent in areas in which resources are abundant and extends the search to a larger area when resources become scarce. We demonstrate that dopaminergic and glutamatergic signaling contribute to the neural circuit controlling ARS in the nematode Caenorhabditis elegans. Ablation of dopaminergic neurons eliminated ARS behavior, as did application of the dopamine receptor antagonist raclopride. Furthermore, ARS was affected by mutations in the glutamate receptor subunits GLR-1 and GLR-2 and the EAT-4 glutamate vesicular transporter. Interestingly, preincubation on dopamine restored the behavior in worms with defective dopaminergic signaling, but not in glr-1, glr-2, or eat-4 mutants. This suggests that dopaminergic and glutamatergic signaling function in the same pathway to regulate turn frequency. Both GLR-1 and GLR-2 are expressed in the locomotory control circuit that modulates the direction of locomotion in response to sensory stimuli and the duration of forward movement during foraging. We propose a mechanism for ARS in C. elegans in which dopamine, released in response to food, modulates glutamatergic signaling in the locomotory control circuit, thus resulting in an increased turn frequency.

The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion

The N-methyl-D-aspartate (NMDA) subtype of glutamate receptor is important for synaptic plasticity and nervous system development and function. We have used genetic and electrophysiological methods to demonstrate that NMR-1, a Caenorhabditis elegans NMDA-type ionotropic glutamate receptor subunit, plays a role in the control of movement and foraging behavior. nmr-1 mutants show a lower probability of switching from forward to backward movement and a reduced ability to navigate a complex environment. Electrical recordings from the interneuron AVA show that NMDA-dependent currents are selectively disrupted in nmr-1 mutants. We also show that a slowly desensitizing variant of a non-NMDA receptor can rescue the nmr-1 mutant phenotype. We propose that NMDA receptors in C. elegans provide long-lived currents that modulate the frequency of movement reversals during foraging behavior.

Animal Foraging and the Evolution of Goal-Directed Cognition

Foraging- and feeding-related behaviors across eumetazoans share similar molecular mechanisms, suggesting the early evolution of an optimal foraging behavior called area-restricted search (ARS), involving mechanisms of dopamine and glutamate in the modulation of behavioral focus. Similar mechanisms in the vertebrate basal ganglia control motor behavior and cognition and reveal an evolutionary progression toward increasing internal connections between prefrontal cortex and striatum in moving from amphibian to primate. The basal ganglia in higher vertebrates show the ability to transfer dopaminergic activity from unconditioned stimuli to conditioned stimuli. The evolutionary role of dopamine in the modulation of goal-directed behavior and cognition is further supported by pathologies of human goal-directed cognition, which have motor and cognitive dysfunction and organize themselves, with respect to dopaminergic activity, along the gradient described by ARS, from perseverative to unfocused. The evidence strongly supports the evolution of goal-directed cognition out of mechanisms initially in control of spatial foraging but, through increasing cortical connections, eventually used to forage for information.

Optimal foraging in semantic memory

Do humans search in memory using dynamic local-to-global search strategies similar to those that animals use to forage between patches in space? If so, do their dynamic memory search policies correspond to optimal foraging strategies seen for spatial foraging? Results from a number of fields suggest these possibilities, including the shared structure of the search problems-searching in patchy environments-and recent evidence supporting a domain-general cognitive search process. To investigate these questions directly, we asked participants to recover from memory as many animal names as they could in 3 min. Memory search was modeled over a representation of the semantic search space generated from the BEAGLE memory model of Jones and Mewhort (2007), via a search process similar to models of associative memory search (e.g., Raaijmakers & Shiffrin, 1981). We found evidence for local structure (i.e., patches) in memory search and patch depletion preceding dynamic local-to-global transitions between patches. Dynamic models also significantly outperformed nondynamic models. The timing of dynamic local-to-global transitions was consistent with optimal search policies in space, specifically the marginal value theorem (Charnov, 1976), and participants who were more consistent with this policy recalled more items.

Longitudinal Analysis of Early Semantic Networks Preferential Attachment or Preferential Acquisition

Analyses of adult semantic networks suggest a learning mechanism involving preferential attachment: A word is more likely to enter the lexicon the more connected the known words to which it is related. We introduce and test two alternative growth principles: preferential acquisition—words enter the lexicon not because they are related to well-connected words, but because they connect well to other words in the learning environment—and the lure of the associates—new words are favored in proportion to their connections with known words. We tested these alternative principles using longitudinal analyses of developing networks of 130 nouns children learn prior to the age of 30 months. We tested both networks with links between words represented by features and networks with links represented by associations. The feature networks did not predict age of acquisition using any growth model. The associative networks grew by preferential acquisition, with the best model incorporating word frequency, number of phonological neighbors, and connectedness of the new word to words in the learning environment, as operationalized by connectedness to words typically acquired by the age of 30 months.

Exploration versus exploitation in space, mind, and society

Search is a ubiquitous property of life. Although diverse domains have worked on search problems largely in isolation, recent trends across disciplines indicate that the formal properties of these problems share similar structures and, often, similar solutions. Moreover, internal search (e.g., memory search) shows similar characteristics to external search (e.g., spatial foraging), including shared neural mechanisms consistent with a common evolutionary origin across species. Search problems and their solutions also scale from individuals to societies, underlying and constraining problem solving, memory, information search, and scientific and cultural innovation. In summary, search represents a core feature of cognition, with a vast influence on its evolution and processes across contexts and requiring input from multiple domains to understand its implications and scope.

Information Search in Decisions From Experience Do Our Patterns of Sampling Foreshadow Our Decisions

Do different patterns of sampling influence the decisions people make, even when the information the decisions are based on is equivalent? Do more and less switching between options correlate with different kinds of decision policies? In past research, the correspondence between search and decision patterns has been difficult to ascertain because the information obtained has often been confounded with its consequences in an exploration-exploitation trade-off. We used a sampling task in which information is explored prior to being exploited. We found that search patterns did reveal decision policies. Individuals who transitioned more frequently between options were more likely to choose options that win most of the time in round-wise comparisons and were more likely to underweight rare, risky events. Less switching between options was associated with choosing options that win in the long run on the basis of summary comparisons—decisions consistent with expected-value maximization and linear weighting of outcomes.

Small Worlds and Semantic Network Growth in Typical and Late Talkers

Network analysis has demonstrated that systems ranging from social networks to electric power grids often involve a small world structure-with local clustering but global ac cess. Critically, small world structure has also been shown to characterize adult human semantic networks. Moreover, the connectivity pattern of these mature networks is consistent with lexical growth processes in which children add new words to their vocabulary based on the structure of the language-learning environment. However, thus far, there is no direct evidence that a childs individual semantic network structure is associated with their early language learning. Here we show that, while typically developing childrens early networks show small world structure as early as 15 months and with as few as 55 words, children with language delay (late talkers) have this structure to a smaller degree. This implicates a maladaptive bias in word acquisition for late talkers, potentially indicating a preference for “oddball” words. The findings provide the first evidence of a link between small-world connectivity and lexical development in individual children.

Search in External and Internal Spaces Evidence for Generalized Cognitive Search Processes

There is compelling molecular and behavioral evidence that goal-directed cognition is an evolutionary descendant of spatial-foraging behavior. Across animal species, similar dopaminergic processes modulate between exploratory and exploitative foraging behaviors and control attention. Consequently, we hypothesized that spatialforaging activity could prime attentional cognitive activity. We examined how searching in physical space influences subsequent search in abstract cognitive space by presenting participants with a spatial-foraging task followed by a repeated Scrabble task involving search for words that could be made from letter sets. Participants who searched through clumpier distributions in space behaved as if words were more densely clumped in the Scrabble task. This was not a function of arousal, but was consistent with predictions of optimal-foraging theory. Furthermore, individual differences in exploratory search were conserved across the two types of tasks. Along with the biological evidence, our results support the idea that there are generalized cognitive search processes.

The Central Executive as a Search Process: Priming Exploration and Exploitation across Domains

The trade-off between exploration and exploitation is common to a wide variety of problems involving search in space and mind. The prevalence of this trade-off and its neurological underpinnings led us to propose domain-general cognitive search processes (Hills, Todd, & Goldstone, 2008). We propose further that these are consistent with the idea of a central executive search process that combines goal-handling across subgoal hierarchies. In the present study, we investigate 3 aspects of this proposal. First, the existence of a unitary central executive search process should allow priming from 1 search task to another and at multiple hierarchical levels. We confirm this by showing cross-domain priming from a spatial search task to 2 different cognitive levels within a lexical search task. Second, given the neural basis of the proposed generalized cognitive search process and the evidence that the central executive is primarily engaged during complex tasks, we hypothesize that priming should require search in the sense of a self-regulated making and testing of sequential predictions about the world. This was confirmed by showing that when participants were allowed to collect spatial resources without searching for them, no priming occurred. Finally, we provide a mechanism for the underlying search process and investigate 3 alternative hypotheses for subgoal hierarchies using the central executive as a search process model (CESP). CESP envisions the central executive as having both emergent and unitary processes, with one of its roles being a generalized cognitive search process that navigates goal hierarchies by mediating persistence on and switching between subgoals.