Independent neural coding of reward and movement by pedunculopontine tegmental nucleus neurons in freely navigating rats: Reward and movement codes of PPTg neurons

Norton, Alix B. W.; Jo, Yong Sang; Clark, Emily W.; Taylor, Cortney A.; Mizumori, Sheri J. Y.

doi:10.1111/j.1460-9568.2011.07649.x

Cited by 66Neurotransmitter Receptor Influence on BehaviorMemory and Neural MechanismsNeural and Behavioral Psychology Studies

Independent neural coding of reward and movement by pedunculopontine tegmental nucleus neurons in freely navigating rats: Reward and movement codes of PPTg neurons

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Norton, Alix B. W., Jo, Yong Sang, Clark, Emily W., Taylor, Cortney A., Mizumori, Sheri J. Y.·2011·European Journal of Neuroscience

DOI 10.1111/j.1460-9568.2011.07649.xPMC PMC3095748

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Abstract

Phasic firing of dopamine (DA) neurons in the ventral tegmental area (VTA) and substantia nigra (SN) is likely to be crucial for reward processing that guides learning. One of the key structures implicated in the regulation of this DA burst firing is the pedunculopontine tegmental nucleus (PPTg), which projects to both the VTA and SN. Different literatures suggest that the PPTg serves as a sensory-gating area for DA cells or it regulates voluntary movement. This study recorded PPTg single-unit activity as rats perform a spatial navigation task to examine the potential for both reward and movement contributions. PPTg cells showed significant changes in firing relative to reward acquisition, the velocity of movement across the maze and turning behaviors of the rats. Reward, but not movement, correlates were impacted by changes in context, and neither correlate type was affected by reward manipulations (e.g. changing the expected location of a reward). This suggests that the PPTg conjunctively codes both reward and behavioral information, and that the reward information is processed in a context-dependent manner. The distinct anatomical distribution of reward and movement cells emphasizes different models of synaptic control by PPTg of DA burst firing in the VTA and SN. Relevant to both VTA and SN learning systems, however, PPTg appears to serve as a sensory gating mechanism to facilitate reinforcement learning, while at the same time provides reinforcement-based guidance of ongoing goal-directed behaviors.

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The PPTg acts as a gate for salient sensory information associated with reward and/or requiring movement.
“These observations have led to the idea that the PPtg acts as a gate for salient sensory information associated with reward and/or requiring movement (Norton et al., 2011).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Norton et al., 2011

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Predictive reward signal of dopamine neurons
Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.1 · Cited by 4,564 · see citing works
The hippocampal-VTA loop: controlling the entry of information into long-term memory
Lisman, J. E., & Grace, A. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.002 · Cited by 1,983 · see citing works
Lateral habenula as a source of negative reward signals in dopamine neurons
Matsumoto, M., & Hikosaka, O. (2007) · Nature · doi:10.1038/nature05860 · Cited by 1,292 · see citing works
Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission
Floresco, S. B., West, A. R., Ash, B., Moore, H., & Grace, A. A. (2003) · Nature Neuroscience · doi:10.1038/nn1103 · Cited by 1,106 · see citing works
Cholinergic systems in mammalian brain and spinal cord
WOOLF, N. (1991) · Progress in Neurobiology · doi:10.1016/0301-0082(91)90006-m · Cited by 948 · see citing works
The pedunculopontine nucleus and Parkinson's disease
Pahapill, P. A. (2000) · Brain · doi:10.1093/brain/123.9.1767 · Cited by 832 · see citing works
The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum
Joel, D., & Weiner, I. (2000) · Neuroscience · doi:10.1016/s0306-4522(99)00575-8 · Cited by 614 · see citing works
Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: A retro‐ and antero‐grade transport and immunohistochemical study
Semba, K., & Fibiger, H. C. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903230307 · Cited by 544 · see citing works
Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat
Wang, H., & Morales, M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06576.x · Cited by 478 · see citing works
Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents
Groenewegen, H. J., Berendse, H. W., & Haber, S. N. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90115-v · Cited by 456 · see citing works
Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior
Zweifel, L. S., Parker, J. G., Lobb, C. J., Rainwater, A., Wall, V. Z., Fadok, J. P., Darvas, M., Kim, M. J., Mizumori, S. J. Y., Paladini, C. A., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813415106 · Cited by 426 · see citing works
Self-citation
Medullary and spinal efferents of the pedunculopontine tegmental nucleus and adjacent mesopontine tegmentum in the rat
Rye, D. B., Lee, H. J., Saper, C. B., & Wainer, B. H. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902690302 · Cited by 424 · see citing works
Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area
Oakman, S., Faris, P. L., Kerr, P., Cozzari, C., & Hartman, B. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-09-05859.1995 · Cited by 384 · see citing works
Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family?
Mena‐Segovia, J., Bolam, J. P., & Magill, P. J. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.07.009 · Cited by 349 · see citing works
Anatomical Substrates for Glutamate‐Dopamine Interactions
Sesack, S., Carr, D. B., Omelchenko, N., & Pinto, A. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.066 · Cited by 348 · see citing works
The pedunculopontine nucleus—Auditory input, arousal and pathophysiology
Reese, N. B., García‐Rill, E., & Skinner, R. D. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(95)00023-o · Cited by 235 · see citing works
Learning-Related Development of Context-Specific Neuronal Responses to Places and Events: The Hippocampal Role in Context Processing
Smith, D. M., & Mizumori, S. J. Y. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3234-05.2006 · Cited by 234 · see citing works
Self-citation
Glutamatergic and cholinergic inputs from the pedunculopontine tegmental nucleus to dopamine neurons in the substantia nigra pars compacta
Futami, T., Takakusaki, K., & Kitai, S. T. (1995) · Neuroscience Research · doi:10.1016/0168-0102(94)00869-h · Cited by 230 · see citing works
Locomotion-inducing sites in the vicinity of the pedunculopontine nucleus
García‐Rill, E., Houser, C. R., Skinner, R. D., Smith, W. L., & Woodward, D. J. (1987) · Brain Research Bulletin · doi:10.1016/0361-9230(87)90208-5 · Cited by 226 · see citing works
Pedunculopontine Tegmental Nucleus Controls Conditioned Responses of Midbrain Dopamine Neurons in Behaving Rats
Pan, W. X., & Hyland, B. I. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0277-05.2005 · Cited by 209 · see citing works
Lesions of the dorsomedial nucleus of the thalamus, medial prefrontal cortex and pedunculopontine nucleus: effects on locomotor activity mediated by nucleus accumbens-ventral pallidal circuitry
Swerdlow, N. R., & Koob, G. F. (1987) · Brain Research · doi:10.1016/0006-8993(87)91129-2 · Cited by 208 · see citing works
Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat
Bevan, M. D., & Bolam, J. P. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07105.1995 · Cited by 203 · see citing works
How best to consider the structure and function of the pedunculopontine tegmental nucleus: Evidence from animal studies
Winn, P. (2006) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2006.05.036 · Cited by 189 · see citing works
Pedunculopontine tegmental stimulation evokes striatal dopamine efflux by activation of acetylcholine and glutamate receptors in the midbrain and pons of the rat
Forster, G. L., & Blaha, C. D. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02511.x · Cited by 175 · see citing works
Cholinergic modulation of midbrain dopaminergic systems
Mena‐Segovia, J., Winn, P., & Bolam, J. P. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.02.003 · Cited by 170 · see citing works
A cholinergic projection to the rat substantia nigra from the pedunculopontine tegmental nucleus
Beninato, M., & Spencer, R. F. (1987) · Brain Research · doi:10.1016/0006-8993(87)91455-7 · Cited by 168 · see citing works
The cholinergic mesopontine tegmentum is a relatively neglected nicotinic master modulator of the dopaminergic system: relevance to drugs of abuse and pathology
Maskos, U. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.5 · Cited by 139 · see citing works
Different Pedunculopontine Tegmental Neurons Signal Predicted and Actual Task Rewards
Okada, K., Toyama, K., Inoue, Y., Isa, T., & Kobayashi, Y. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4415-08.2009 · Cited by 138 · see citing works
Stimulation of the pedunculopontine tegmental nucleus in the rat produces burst firing in A9 dopaminergic neurons
Lokwan, S. J. A., Overton, P. G., Berry, M. S., & Clark, D. T. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00748-9 · Cited by 129 · see citing works
Parallel processing across neural systems: Implications for a multiple memory system hypothesis
Mizumori, S. J. Y., Yeshenko, O., Gill, K. M., & Davis, D. M. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.07.007 · Cited by 124 · see citing works
Self-citation
Pedunculopontine-evoked excitation of substantia nigra neurons in the rat
Scarnati, E., Campana, E., & Pacitti, C. (1984) · Brain Research · doi:10.1016/0006-8993(84)90339-1 · Cited by 121 · see citing works
GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories
Mena‐Segovia, J., Micklem, B. R., Nair‐Roberts, R. G., Ungless, M. A., & Bolam, J. P. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22065 · Cited by 120 · see citing works
Separate neuronal populations of the rat globus pallidus projecting to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental area
Moriizumi, T., & Hattori, T. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90156-v · Cited by 113 · see citing works
Sensory-motor gating and cognitive control by the brainstem cholinergic system
Kobayashi, Y., & Isa, T. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00059-x · Cited by 108 · see citing works
Two types of cholinergic neurons in the rat tegmental pedunculopontine nucleus: electrophysiological and morphological characterization
Takakusaki, K., Shiroyama, T., & Kitai, S. T. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00019-5 · Cited by 105 · see citing works
Contribution of Pedunculopontine Tegmental Nucleus Neurons to Performance of Visually Guided Saccade Tasks in Monkeys
Kobayashi, Y., Inoue, Y., Yamamoto, M., Isa, T., & Aizawa, H. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.2.715 · Cited by 104 · see citing works
Outflow from the nucleus accumbens to the pedunculopontine tegmental nucleus: A dissociation between locomotor activity and the acquisition of responding for conditioned reinforcement stimulated by d-amphetamine
Inglis, W. L., Dunbar, J. S., & Winn, P. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90314-x · Cited by 99 · see citing works
The role of the pedunculopontine tegmental nucleus in relation to conditioned motor performance in the cat
Dormont, J. F., Condé, H., & Farin, D. (1998) · Experimental Brain Research · doi:10.1007/s002210050474 · Cited by 92 · see citing works
Locomotor projections from the pedunculopontine nucleus to the spinai cord
Skinner, R. D., Kinjo, N., Henderson, V., & García‐Rill, E. (1990) · Neuroreport · doi:10.1097/00001756-199011000-00001 · Cited by 91 · see citing works
Examination of the role of the pedunculopontine tegmental nucleus in radial maze tasks with or without a delay
Keating, G. L., & Winn, P. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00108-2 · Cited by 80 · see citing works
Ventral tegmental area disruption selectively affects CA1/CA2 but not CA3 place fields during a differential reward working memory task
Martig, A. K., & Mizumori, S. J. Y. (2010) · Hippocampus · doi:10.1002/hipo.20734 · Cited by 71 · see citing works
Self-citation
Conjunctive encoding of movement and reward by ventral tegmental area neurons in the freely navigating rodent.
Puryear, C. B., Kim, M. J., & Mizumori, S. J. Y. (2010) · Behavioral Neuroscience · doi:10.1037/a0018865 · Cited by 69 · see citing works
Self-citation
Further evidence for segregated output channels from superior colliculus in rat: ipsilateral tecto-pontine and tecto-cuneiform projections have different cells of origin
Redgrave, P., Mitchell, I. J., & Dean, P. (1987) · Brain Research · doi:10.1016/0006-8993(87)90165-x · Cited by 64 · see citing works
Basal ganglia contributions to adaptive navigation
Mizumori, S. J. Y., Puryear, C. B., & Martig, A. K. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.014 · Cited by 63 · see citing works
Self-citation
In vivo electrophysiological distinction of histochemically-identified cholinergic neurons using extracellular recording and labelling in rat laterodorsal tegmental nucleus
Koyama, Y., Honda, T., Kusakabe, M., Kayama, Y., & Sugiura, Y. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00439-9 · Cited by 61 · see citing works
Bar pressing for food: differential consequences of lesions to the anterior versus posterior pedunculopontine
Wilson, D. I. G., MacLaren, D. A. A., & Winn, P. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06836.x · Cited by 57 · see citing works
Intravenous self‐administration of nicotine is altered by lesions of the posterior, but not anterior, pedunculopontine tegmental nucleus
Alderson, H. L., Latimer, M. P., & Winn, P. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04737.x · Cited by 57 · see citing works
A functional dissociation of the anterior and posterior pedunculopontine tegmental nucleus: excitotoxic lesions have differential effects on locomotion and the response to nicotine
Alderson, H. L., Latimer, M. P., & Winn, P. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0174-4 · Cited by 54 · see citing works
Effects of ibotenate pedunculopontine tegmental nucleus lesions on exploratory behaviour in the open field
Steiniger, B., & Kretschmer, B. D. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.08.001 · Cited by 40 · see citing works
Excitotoxic lesions of the pedunculopontine tegmental nucleus disinhibit orofacial behaviours stimulated by microinjections of d-amphetamine into rat ventrolateral caudate-putamen
Allen, L. F., & Winn, P. (1995) · Experimental Brain Research · doi:10.1007/bf00242012 · Cited by 32 · see citing works
Context-dependent modulation by D₁ receptors: Differential effects in hippocampus and striatum.
Gill, K. M., & Mizumori, S. J. Y. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.2.377 · Cited by 27 · see citing works
Self-citation
Specific changes in hippocampal spatial codes predict spatial working memory performance
Puryear, C. B., King, M. A., & Mizumori, S. J. Y. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.12.007 · Cited by 16 · see citing works
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Authors: Norton, A. B. W., Jo, Y. S., Clark, E. W., Taylor, C. A., & Mizumori, S. J. Y.
Affiliations: University of Washington (US)
Corresponding author: Mizumori, Sheri J. Y.
ORCID: Norton, Alix B. W.
Jo, Yong Sang
Mizumori, Sheri J. Y.
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 2011-03-14
Volume: 33
Issue: 10
Pages: 1885-1896
ISSN: 0953-816X (ISSN-L)
DOI: 10.1111/j.1460-9568.2011.07649.x
PMC: PMC3095748
OpenAlex: W1554587170
Cited by: 66
References: 52
Citations by year: 2026: 3 · 2025: 3 · 2024: 5 · 2023: 3 · 2022: 4 · 2021: 2 · 2020: 2 · 2019: 2 · 2018: 4 · 2017: 6 · 2016: 11 · 2015: 7 · 2014: 7 · 2013: 5 · 2012: 1
FWCI: 1.85
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: doi.wiley.com/10.1002/tdm_license_1.1 (tdm, 1632 d)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R56MH058755, MH-58755, R01MH058755)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: pedunculopontine nucleus, reward coding, single-unit activity, spatial navigation, sensory gating, reinforcement learning, goal-directed behavior, substantia nigra, ventral tegmental area, dopaminergic neurons, rats
MeSH terms: Action Potentials, Animals, Behavior, Animal, Dopamine, Male, Movement, Neurons, Reward, Spatial Behavior, Rats, Long-Evans, Pedunculopontine Tegmental Nucleus, Rats

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Independent neural coding of reward and movement by pedunculopontine tegmental nucleus neurons in freely navigating rats: Reward and movement codes of PPTg neurons

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