Electrophysiological evidence for functionally distinct neuronal populations in the human substantia nigra

Ramayya, Ashwin G.; Zaghloul, Kareem A.; Weidemann, Christoph T.; Baltuch, Gordon H.; Kahana, Michael J.

doi:10.3389/fnhum.2014.00655

Cited by 20 publications

(36 citation statements)

References 41 publications

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“…We found that MS neurons were on average characterized by longer waveforms compared to non-MS neurons (1.15 ± 0.23 ms versus 0.96 ± 0.32 ms; waveform length was measured as the time that elapsed between the two positive peaks [ 14 ] of the waveform; t [65] = 2.65, p = 0.012, permutation t test; Figures 3H and 3I ). Additionally, MS neurons satisfied the criteria for DA neurons established by previous work: 15/17 MS neurons had waveforms longer than 0.8 ms and firing rates lower than 15 Hz [ 14 , 41 ]. We also found that the recording sites where MS neurons were identified were predominantly in the dorsal parts of the SN ( Figures 1D and 1E ).…”

Section: Resultsmentioning

confidence: 78%

Novelty-Sensitive Dopaminergic Neurons in the Human Substantia Nigra Predict Success of Declarative Memory Formation

et al. 2018

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Summary The encoding of information into long-term declarative memory is facilitated by dopamine. This process depends on hippocampal novelty signals, but it remains unknown how midbrain dopaminergic neurons are modulated by declarative-memory-based information. We recorded individual substantia nigra (SN) neurons and cortical field potentials in human patients performing a recognition memory task. We found that 25% of SN neurons were modulated by stimulus novelty. Extracellular waveform shape and anatomical location indicated that these memory-selective neurons were putatively dopaminergic. The responses of memory-selective neurons appeared 527 ms after stimulus onset, changed after a single trial, and were indicative of recognition accuracy. SN neurons phase locked to frontal cortical theta-frequency oscillations, and the extent of this coordination predicted successful memory formation. These data reveal that dopaminergic neurons in the human SN are modulated by memory signals and demonstrate a progression of information flow in the hippocampal-basal ganglia-frontal cortex loop for memory encoding.

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Section: Resultsmentioning

confidence: 78%

Novelty-Sensitive Dopaminergic Neurons in the Human Substantia Nigra Predict Success of Declarative Memory Formation

et al. 2018

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“…In a previous study, we showed that SN single-units that demonstrated firing rates slower than 15 Hz and waveform durations >0.8 ms demonstrated post-feedback responses consistent with DA neurons, whereas units that demonstrated high spike rates (>15 Hz) and narrow waveforms (<0.8 ms) demonstrated post-feedback responses consistent with GABAergic neurons (Ramayya et al, 2014b), a finding consistent with prior non-human primate studies (Matsumoto and Hikosaka, 2009). …”

Section: Methodsmentioning

confidence: 85%

Proximity of Substantia Nigra Microstimulation to Putative GABAergic Neurons Predicts Modulation of Human Reinforcement Learning

Ramayya

Pedisich

Levy

et al. 2017

Front. Hum. Neurosci.

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Neuronal firing in the substantia nigra (SN) immediately following reward is thought to play a crucial role in human reinforcement learning. As in Ramayya et al. (2014a) we applied microstimulation in the SN of patients undergoing deep brain stimulation (DBS) for the treatment of Parkinson's disease as they engaged in a two-alternative reinforcement learning task. We obtained microelectrode recordings to assess the proximity of the electrode tip to putative dopaminergic and GABAergic SN neurons and applied stimulation to assess the functional importance of these neuronal populations for learning. We found that the proximity of SN microstimulation to putative GABAergic neurons predicted the degree of stimulation-related changes in learning. These results extend previous work by supporting a specific role for SN GABA firing in reinforcement learning. Stimulation near these neurons appears to dampen the reinforcing effect of rewarding stimuli.

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“…Third, whereas molecular analysis of STN and GPi-obtained BTIs may be of interest to investigate functional changes occurring in PD, other structures bearing alpha-synuclein pathology, like the SNpc, might be more relevant to address pathogenesis. Indeed, because the SN lies anatomically just below the STN, it is not unusual for the tip of the DBS electrode to be placed within the SN [ 33 ], and we therefore assume that BTIs can also be captured from this pivotal structure in certain patients.…”

Section: Discussionmentioning

confidence: 99%

Deep brain stimulation-associated brain tissue imprints: a new in vivo approach to biological research in human Parkinson’s disease

Zaccaria

Bouamrani

Chabardès

et al. 2016

Mol Neurodegeneration

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BackgroundDeep brain stimulation (DBS) of the subthalamic nucleus (STN) or the internal segment of the globus pallidus (GPi) has been established as a highly effective symptomatic therapy for Parkinson’s disease (PD). An intriguing biological aspect related to the DBS procedure is that a temporary contact establishes between surgical instruments and the surrounding brain tissue. In this exploratory study, we took advantage of this unique context to harvest brain material adhering to the stylet routinely used during surgery, and to examine the biological value of these samples, here referred to as “brain tissue imprints” (BTIs).ResultsNineteen BTIs from 12 STN- or GPi-electrode implanted patients were obtained in vivo during DBS surgery, without any modification of the surgical procedure. Immunofluorescence analyses confirmed that our approach allowed the harvesting of many neural cells including neurons harboring distinct neurotransmitter markers. Shotgun proteomic and transcriptomic analyses provided for the first time molecular information from DBS-associated brain samples, and confirmed the compatibility of this new type of sample with poly-omic approaches. The method appears to be safe and results consistent.ConclusionsWe here propose BTIs as original and highly valuable brain samples, and DBS-related brain imprinting as a new conceptual approach to biological research in living patients with PD.Electronic supplementary materialThe online version of this article (doi:10.1186/s13024-016-0077-4) contains supplementary material, which is available to authorized users.

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Electrophysiological evidence for functionally distinct neuronal populations in the human substantia nigra

Cited by 20 publications

References 41 publications

Novelty-Sensitive Dopaminergic Neurons in the Human Substantia Nigra Predict Success of Declarative Memory Formation

Novelty-Sensitive Dopaminergic Neurons in the Human Substantia Nigra Predict Success of Declarative Memory Formation

Proximity of Substantia Nigra Microstimulation to Putative GABAergic Neurons Predicts Modulation of Human Reinforcement Learning

Deep brain stimulation-associated brain tissue imprints: a new in vivo approach to biological research in human Parkinson’s disease

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