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The Journal of Neuroscience : the... May 2020Rodents can successfully learn multiple novel stimulus-response associations after only a few repetitions when the contingencies predict reward. The circuits modified...
Rodents can successfully learn multiple novel stimulus-response associations after only a few repetitions when the contingencies predict reward. The circuits modified during such reinforcement learning to support decision-making are not known, but the olfactory tubercle (OT) and posterior piriform cortex (pPC) are candidates for decoding reward category from olfactory sensory input and relaying this information to cognitive and motor areas. Through single-cell recordings in behaving male and female C57BL/6 mice, we show here that an explicit representation for reward category emerges in the OT within minutes of learning a novel odor-reward association, whereas the pPC lacks an explicit representation even after weeks of overtraining. The explicit reward category representation in OT is visible in the first sniff (50-100 ms) of an odor on each trial, and precedes the motor action. Together, these results suggest that the coding of stimulus information required for reward prediction does not occur within olfactory cortex, but rather in circuits involving the olfactory striatum. Rodents are olfactory specialists and can use odors to learn contingencies quickly and well. We have found that mice can readily learn to place multiple odors into rewarded and unrewarded categories. Once they have learned the rule, they can do such categorization in a matter of minutes (<10 trials). We found that neural activity in olfactory cortex largely reflects sensory coding, with very little explicit information about categories. By contrast, neural activity in a brain region in the ventral striatum is rapidly modified in a matter of minutes to reflect reward category. Our experiments set up a paradigm for studying rapid sensorimotor reinforcement in a circuit that is right at the interface of sensory input and reward areas.
Topics: Animals; Female; Male; Mice; Mice, Inbred C57BL; Neurons; Olfactory Perception; Olfactory Tubercle; Piriform Cortex; Reward
PubMed: 32321744
DOI: 10.1523/JNEUROSCI.2604-19.2020 -
BMC Neuroscience May 2005The dentate gyrus is well known for its mossy fiber projection to the hippocampal field 3 (CA3) and its extensive associational and commissural connections. The dentate... (Comparative Study)
Comparative Study
BACKGROUND
The dentate gyrus is well known for its mossy fiber projection to the hippocampal field 3 (CA3) and its extensive associational and commissural connections. The dentate gyrus, on the other hand, has only few projections to the CA1 and the subiculum, and none have clearly been shown to extrahippocampal target regions.
RESULTS
Using anterograde and retrograde tracer techniques in the Madagascan lesser hedgehog tenrec (Afrosoricidae, Afrotheria) it was shown in this study that the dentate hilar region gave rise to a faint, but distinct, bilateral projection to the most rostromedial portion of the olfactory tubercle, particularly its molecular layer. Unlike the CA1 and the subiculum the dentate gyrus did not project to the accumbens nucleus. A control injection into the medial septum-diagonal band complex also retrogradely labeled cells in the dentate hilus, but these neurons were found immediately adjacent to the heavily labeled CA3, while the tracer injections into the rostromedial tubercle did not reveal any labeling in CA3.
CONCLUSION
The dentate hilar neurons projecting to the olfactory tubercle cannot be considered displaced cells of CA3 but represent true dentato-tubercular projection neurons. This projection supplements the subiculo-tubercular projection. Both terminal fields overlap among one another as well as with the fiber terminations arising in the anteromedial frontal cortex. The rostromedial olfactory tubercle might represent a distinct ventral striatal target area worth investigating in studies of the parallel processing of cortico-limbic information in tenrec as well as in cat and monkey.
Topics: Animals; Dentate Gyrus; Eulipotyphla; Hippocampus; Neural Pathways; Olfactory Pathways
PubMed: 15927048
DOI: 10.1186/1471-2202-6-38 -
The Journal of Neuroscience : the... Oct 2003Cocaine has multiple actions and multiple sites of action in the brain. Evidence from pharmacological studies indicates that it is the ability of cocaine to block...
Cocaine has multiple actions and multiple sites of action in the brain. Evidence from pharmacological studies indicates that it is the ability of cocaine to block dopamine uptake and elevate extracellular dopamine concentrations, and thus increase dopaminergic receptor activation, that makes cocaine rewarding. Lesion studies have implicated the nucleus accumbens (the dorsal portion of the "ventral striatum") as the probable site of the rewarding action of the drug. However, the drug is only marginally self-administered into this site. We now report that cocaine (60 or 200 mm in 75 nl/infusion) is readily self-administered into the olfactory tubercle, the most ventral portion of the ventral striatum. Cocaine (200 mm) was self-administered marginally into the accumbens shell but not into the core, dorsal striatum, or ventral pallidum. In addition, cocaine injections (200 mm in 300 nl) into the tubercle but not the shell or ventral pallidum induced conditioned place preference. Rewarding effects of cocaine in the tubercle were blocked by coadministration of dopamine D1 or D2 antagonists (1 mm SCH 23390 or 3 mm raclopride) and were not mimicked by injections of the local anesthetic procaine (800 mm). In conclusion, the tubercle plays a critical role in mediating rewarding action of cocaine.
Topics: Anesthetics, Local; Animals; Behavior, Animal; Choice Behavior; Cocaine; Cocaine-Related Disorders; Discrimination, Psychological; Dopamine Antagonists; Dopamine D2 Receptor Antagonists; Drug Administration Routes; Male; Olfactory Pathways; Rats; Rats, Wistar; Receptors, Dopamine D1; Reinforcement, Psychology; Reward; Self Administration
PubMed: 14561857
DOI: 10.1523/JNEUROSCI.23-28-09305.2003 -
The Journal of Neuroscience : the... Jan 2016The ventral striatum is critical for evaluating reward information and the initiation of goal-directed behaviors. The many cellular, afferent, and efferent similarities...
UNLABELLED
The ventral striatum is critical for evaluating reward information and the initiation of goal-directed behaviors. The many cellular, afferent, and efferent similarities between the ventral striatum's nucleus accumbens and olfactory tubercle (OT) suggests the distributed involvement of neurons within the ventral striatopallidal complex in motivated behaviors. Although the nucleus accumbens has an established role in representing goal-directed actions and their outcomes, it is not known whether this function is localized within the nucleus accumbens or distributed also within the OT. Answering such a fundamental question will expand our understanding of the neural mechanisms underlying motivated behaviors. Here we address whether the OT encodes natural reinforcers and serves as a substrate for motivational information processing. In recordings from mice engaged in a novel water-motivated instrumental task, we report that OT neurons modulate their firing rate during initiation and progression of the instrumental licking behavior, with some activity being internally generated and preceding the first lick. We further found that as motivational drive decreases throughout a session, the activity of OT neurons is enhanced earlier relative to the behavioral action. Additionally, OT neurons discriminate the types and magnitudes of fluid reinforcers. Together, these data suggest that the processing of reward information and the orchestration of goal-directed behaviors is a global principle of the ventral striatum and have important implications for understanding the neural systems subserving addiction and mood disorders.
SIGNIFICANCE STATEMENT
Goal-directed behaviors are widespread among animals and underlie complex behaviors ranging from food intake, social behavior, and even pathological conditions, such as gambling and drug addiction. The ventral striatum is a neural system critical for evaluating reward information and the initiation of goal-directed behaviors. Here we show that neurons in the olfactory tubercle subregion of the ventral striatum robustly encode the onset and progression of motivated behaviors, and discriminate the type and magnitude of a reward. Our findings are novel in showing that olfactory tubercle neurons participate in such coding schemes and are in accordance with the principle that ventral striatum substructures may cooperate to guide motivated behaviors.
Topics: Action Potentials; Animals; Appetitive Behavior; Goals; Male; Mice; Mice, Inbred C57BL; Motivation; Neurons; Olfactory Tubercle; Reward; Statistics, Nonparametric; Ventral Striatum
PubMed: 26758844
DOI: 10.1523/JNEUROSCI.3328-15.2016 -
IBRO Reports Dec 2020The tenia tecta is extensively interconnected with the main olfactory bulb and olfactory cortical areas and is well positioned to contribute to olfactory processing....
The tenia tecta is extensively interconnected with the main olfactory bulb and olfactory cortical areas and is well positioned to contribute to olfactory processing. However, little is known about odor representation within its dorsal (DTT) and ventral (VTT) components. To address this need, spontaneous and odor-evoked activity of DTT and VTT neurons was recorded from urethane anesthetized mice and compared to activity recorded from adjacent areas within adjacent caudomedial aspects of the anterior olfactory nucleus (AON). Neurons recorded from DTT, VTT, and AON exhibited odor-selective alterations in firing rate in response to a diverse set of monomolecular odorants. While DTT and AON neurons exhibited similar tuning breadth, selectivity, and response topography, the proportion of odor-selective neurons was substantially higher in the DTT. These findings provide evidence that the tenia tecta may contribute to the encoding of specific stimulus attributes. Further work is needed to fully characterize functional organization of the tenia tecta and its contribution to sensory representation and utilization.
PubMed: 32793841
DOI: 10.1016/j.ibror.2020.07.010 -
The Journal of Comparative Neurology Aug 1994The connections between the olfactory bulb, primary olfactory cortex, and olfactory related areas of the orbital cortex were defined in macaque monkeys with a... (Comparative Study)
Comparative Study
The connections between the olfactory bulb, primary olfactory cortex, and olfactory related areas of the orbital cortex were defined in macaque monkeys with a combination of anterograde and retrograde axonal tracers and electrophysiological recording. Anterograde tracers placed into the olfactory bulb labeled axons in eight primary olfactory cortical areas: the anterior olfactory nucleus, piriform cortex, ventral tenia tecta, olfactory tubercle, anterior cortical nucleus of the amygdala, periamygdaloid cortex, and olfactory division of the entorhinal cortex. The bulbar axons terminate in the outer part of layer I throughout these areas and are most dense in areas that are close to the lateral olfactory tract. Labeled axons also were found in the superficial part of nucleus of the horizontal diagonal band. Retrograde tracers injected into the olfactory bulb labeled cells in the nucleus of the diagonal band and in all of the primary olfactory cortical areas except the olfactory tubercle. Electrical stimulation of the olfactory bulb evoked short-latency unit responses and a characteristic field wave in the primary olfactory cortex. Multiunit activity in layer II tended to be of shorter latency than that in layer III and the endopiriform nucleus. Associational connections within the primary olfactory cortex were demonstrated with anterograde tracer injections into the piriform cortex and the entorhinal cortex. Injections into the piriform cortex near the lateral olfactory tract labeled axons in the deep part of layer I of many primary olfactory areas, but especially in areas near the tract. An injection into the rostral entorhinal cortex, distant to the lateral olfactory tract, labeled a complementary distribution of axons in deep layer I of olfactory areas medial and caudoventral to the tract. This organization resembles that reported in the primary olfactory cortex of the rat [Luskin and Price (1983) J. Comp. Neurol. 216:264-291]. The anterograde tracer injections into the piriform cortex and retrograde tracer injections into the orbital and medial prefrontal cortex and rostral insula label connections from the primary olfactory cortex to nine areas in the caudal orbital cortex, including the agranular insula areas Iam, Iai, Ial, Iapm, and Iapl and areas 14c, 25, 13a, and 13m. The piriform cortex projects most heavily to layer I of these areas. Only Iam, Iapm, and 13a receive a substantial projection to the deeper layers. Areas Iam, Iapm, and 13a were also the only areas that responded with multiunit action potentials to olfactory bulb stimulation in anesthetized animals.(ABSTRACT TRUNCATED AT 400 WORDS)
Topics: Animals; Axonal Transport; Axons; Brain; Brain Mapping; Electric Stimulation; Female; Macaca; Macaca fascicularis; Macaca nemestrina; Male; Nerve Fibers; Olfactory Bulb; Olfactory Pathways; Prefrontal Cortex; Rats; Species Specificity
PubMed: 7527806
DOI: 10.1002/cne.903460306 -
Reviews in the Neurosciences 2012The present paper reviews foundational and contemporary theories of motivated behaviors and the growing body of evidence that they require specific functional... (Review)
Review
The present paper reviews foundational and contemporary theories of motivated behaviors and the growing body of evidence that they require specific functional interactions within the basal ganglia. Such evidence suggests that unconditioned responses (UR), conditioned responses (CR), goal-directed actions and stimulus-response (S-R) habits are selected in the basal ganglia. Such selection depends on activation of striatal neurons by cortical and subcortical neurons encoding unconditioned stimuli (US), conditioned stimuli (CS), goals and neutral stimuli (S). These neurons project respectively to the medial nucleus accumbens (NAc) shell/olfactory tubercle, NAc core/lateral olfactory tubercle, dorsolateral striatum and dorsomedial striatum. The strength of these synapses is altered when the levels of extracellular dopamine in the basal ganglia undergo phasic increases or decreases, which signal outcomes that are, respectively, better or worse than expected. In addition, dopamine release in response to salient USs and to CSs with incentive salience increases the signal-to-noise ratio of corticostriatal neurotransmission, thus 'energizing' the performance of selected actions. Different actions can be selected in the striatum because the striatal neurons of the so-called direct and indirect pathways can respectively initiate and end actions through pallidum/nigral-thalamic projections to premotor and motor areas of the cortex. According to this view, the basal ganglia is thought to play a role in the action-selection processes needed for the expression of both declarative and procedural memories, but the memories of the contexts, predictive stimuli or neutral stimuli associated with free rewards or with an action's outcomes are stored elsewhere.
Topics: Animals; Basal Ganglia; Conditioning, Classical; Humans; Motivation
PubMed: 23079510
DOI: 10.1515/revneuro-2012-0063 -
Brain, Behavior and Evolution 2006This study was undertaken to determine whether the olfactory tubercles of two monotremes (platypus and echidna) showed cyto- or chemoarchitectural differences from the... (Comparative Study)
Comparative Study
This study was undertaken to determine whether the olfactory tubercles of two monotremes (platypus and echidna) showed cyto- or chemoarchitectural differences from the tubercles of therian mammals. Nissl staining was applied in conjunction with enzyme reactivity for NADPH diaphorase and acetylcholinesterase, and immunoreactivity for calcium binding proteins (parvalbumin, calbindin and calretinin) and tyrosine hydroxylase (echidna only). Golgi impregnations of the tubercle were also available for the echidna. The olfactory tubercle is a poorly laminated structure in the echidna, despite the pronounced development of other components of the echidna olfactory system, and the dense cell layer of the olfactory tubercle was found to be discontinuous and irregular. Granule cell clusters (islands of Calleja) were present, but were small, poorly defined and did not show the intense NADPH diaphorase activity seen in marsupial and placental mammals. A putative small island of Calleja magna was seen in only one echidna out of four. In Golgi impregnations of the echidna olfactory tubercle, the most abundant neuron type was a medium-sized densely spined neuron similar to that seen in the olfactory tubercle of some therians. Large spine-poor neurons were also seen in the polymorphic layer. In the platypus, the olfactory tubercle was very small but showed more pronounced lamination than the echidna, although no granule cell clusters were seen. In both monotremes, the development of the olfactory tubercle was poor relative to other components of the olfactory system (bulb and piriform cortex). The small olfactory tubercle region in the platypus is consistent with poor olfaction in that aquatic mammal, but the tubercle in the echidna is more like that of a microsmatic mammal than other placentals occupying a similar niche (e.g., insectivores).
Topics: Animals; Female; Macropodidae; NADPH Dehydrogenase; Neurons; Olfactory Pathways; Organ Size; Platypus; Tachyglossidae; Tyrosine 3-Monooxygenase
PubMed: 16244467
DOI: 10.1159/000089182 -
Nature Communications Jun 2022Identifying the circuits responsible for cognition and understanding their embedded computations is a challenge for neuroscience. We establish here a hierarchical...
Identifying the circuits responsible for cognition and understanding their embedded computations is a challenge for neuroscience. We establish here a hierarchical cross-scale approach, from behavioral modeling and fMRI in task-performing mice to cellular recordings, in order to disentangle local network contributions to olfactory reinforcement learning. At mesoscale, fMRI identifies a functional olfactory-striatal network interacting dynamically with higher-order cortices. While primary olfactory cortices respectively contribute only some value components, the downstream olfactory tubercle of the ventral striatum expresses comprehensively reward prediction, its dynamic updating, and prediction error components. In the tubercle, recordings reveal two underlying neuronal populations with non-redundant reward prediction coding schemes. One population collectively produces stabilized predictions as distributed activity across neurons; in the other, neurons encode value individually and dynamically integrate the recent history of uncertain outcomes. These findings validate a cross-scale approach to mechanistic investigations of higher cognitive functions in rodents.
Topics: Animals; Cerebral Cortex; Magnetic Resonance Imaging; Mice; Olfactory Tubercle; Reinforcement, Psychology; Reward; Ventral Striatum
PubMed: 35676281
DOI: 10.1038/s41467-022-30978-1 -
Brain Research Jul 1998The goal of this study was to support the hypothesis that visceral signals may integrate and influence behavior by way of direct pathways from the nucleus tractus...
The goal of this study was to support the hypothesis that visceral signals may integrate and influence behavior by way of direct pathways from the nucleus tractus solitarii (NTS) to the olfactory tubercle and the midline/intralaminar thalamus. An anterograde tracer, biotinylated dextran amine (BDA) was iontophoresed bilaterally into the caudal NTS to optimize terminal labeling. NTS-cortical projections traversed both limbs of the diagonal bands providing heavy innervation, and terminated lightly within layer 3 of the olfactory tubercle. NTS-thalamic projections terminated within anterior and, as previously shown, posterior divisions of nucleus paraventricularis thalami and avoided the adjoining mediodorsal thalamic nucleus. Heretofore unrecognized projections were traced to the parafascicular and reuniens thalamic nuclei, and the peripeduncular nucleus. Control experiments identified the nucleus gracilis as the principal source of ascending projections to ventroposterior lateral, posterior and intralaminar thalamic nuclei. Our data corroborate the supposition that olfactory signals may integrate with visceral stimuli in the striatal compartment of olfactory tubercle. NTS projections encompass thalamic nuclei that project topographically to the prefrontal cortex, hippocampus and ventral (limbic) striatum, regions activated by visceral stimulation. Structural data support the idea that compartments of the non-discriminative thalamus may contribute to perception and behavioral responses to visceral stimulation.
Topics: Afferent Pathways; Animals; Behavior, Animal; Biotin; Brain Mapping; Dextrans; Fluorescent Dyes; Olfactory Bulb; Rats; Rats, Sprague-Dawley; Solitary Nucleus; Synaptic Transmission; Thalamus; Viscera
PubMed: 9666113
DOI: 10.1016/s0006-8993(98)00442-9