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Focal Cortical Surface Cooling is a Novel and Safe Method for Intraoperative Functional Brain Mapping

Ibayashi, Kenji; Cardenas, Araceli R; Oya, Hiroyuki; Kawasaki, Hiroto; Kovach, Christopher K; Howard, Matthew A; Long, Michael A; Greenlee, Jeremy D W
OBJECTIVE:Electric cortical stimulation (ECS) has been the gold standard for intraoperative functional mapping in neurosurgery, yet it carries the risk of induced seizures. We assess the safety of focal cortical cooling (CC) as a potential alternative to ECS. METHODS:We reviewed 40 patients (13 with tumor and 27 with mesial temporal lobe epilepsy) who underwent intraoperative CC at the University of Iowa Hospital and Clinics (CC group), of whom 38 underwent ECS preceding CC. Intraoperative and postoperative seizure incidence, postoperative neurologic deficits, and new postoperative radiographic findings were collected to assess CC safety. Fifty-five patients who underwent ECS mapping without CC (ECS-alone group) were reviewed as a control cohort. Another 25 patients who underwent anterior temporal lobectomy (ATL) without CC or ECS (no ECS/no CC-ATL group) were also reviewed to evaluate long-term effects of CC. RESULTS:Seventy-nine brain sites in the CC group were cooled, comprising inferior frontal gyrus (44%), precentral gyrus (39%), postcentral gyrus (6%), subcentral gyrus (4%), and superior temporal gyrus (6%). The incidence of intraoperative seizure(s) was 0% (CC group) and 3.6% (ECS-alone group). The incidence of seizure(s) within the first postoperative week did not significantly differ among CC (7.9%), ECS-alone (9.0%), and no ECS/no CC-ATL groups (12%). There was no significant difference in the incidence of postoperative radiographic change between CC (7.5%) and ECS-alone groups (5.5%). Long-term seizure outcome (Engel I+II) for mesial temporal epilepsy did not differ among CC (80%), ECS-alone (83.3%), and no ECS/no CC-ATL groups (83.3%). CONCLUSIONS:CC when used as an intraoperative mapping technique is safe and may complement ECS.
PMID: 33307258
ISSN: 1878-8769
CID: 4770852

Local Axonal Conduction Shapes the Spatiotemporal Properties of Neural Sequences

Egger, Robert; Tupikov, Yevhen; Elmaleh, Margot; Katlowitz, Kalman A; Benezra, Sam E; Picardo, Michel A; Moll, Felix; Kornfeld, Jörgen; Jin, Dezhe Z; Long, Michael A
Sequential activation of neurons has been observed during various behavioral and cognitive processes, but the underlying circuit mechanisms remain poorly understood. Here, we investigate premotor sequences in HVC (proper name) of the adult zebra finch forebrain that are central to the performance of the temporally precise courtship song. We use high-density silicon probes to measure song-related population activity, and we compare these observations with predictions from a range of network models. Our results support a circuit architecture in which heterogeneous delays between sequentially active neurons shape the spatiotemporal patterns of HVC premotor neuron activity. We gauge the impact of several delay sources, and we find the primary contributor to be slow conduction through axonal collaterals within HVC, which typically adds between 1 and 7.5 ms for each link within the sequence. Thus, local axonal "delay lines" can play an important role in determining the dynamical repertoire of neural circuits.
PMCID:7577554
PMID: 33064989
ISSN: 1097-4172
CID: 4641692

Singing mice

Banerjee, Arkarup; Phelps, Steven M; Long, Michael A
A Quick guide to singing mice.
PMID: 30889384
ISSN: 1879-0445
CID: 3735012

Motor cortical control of vocal interaction in neotropical singing mice

Okobi, Daniel E; Banerjee, Arkarup; Matheson, Andrew M M; Phelps, Steven M; Long, Michael A
Like many adaptive behaviors, acoustic communication often requires rapid modification of motor output in response to sensory cues. However, little is known about the sensorimotor transformations that underlie such complex natural behaviors. In this study, we examine vocal exchanges in Alston's singing mouse (Scotinomys teguina). We find that males modify singing behavior during social interactions on a subsecond time course that resembles both traditional sensorimotor tasks and conversational speech. We identify an orofacial motor cortical region and, via a series of perturbation experiments, demonstrate a hierarchical control of vocal production, with the motor cortex influencing the pacing of singing behavior on a moment-by-moment basis, enabling precise vocal interactions. These results suggest a systems-level framework for understanding the sensorimotor transformations that underlie natural social interactions.
PMID: 30819963
ISSN: 1095-9203
CID: 3698672

Editorial overview: Systems neuroscience [Editorial]

Long, Michael; Cossart, Rosa
PMID: 30217267
ISSN: 1873-6882
CID: 3278452

Morphological characterization of HVC projection neurons in the zebra finch (Taeniopygia guttata)

Benezra, Sam E; Narayanan, Rajeevan T; Egger, Robert; Oberlaender, Marcel; Long, Michael A
Singing behavior in the adult male zebra finch is dependent upon the activity of a cortical region known as HVC (proper name). The vast majority of HVC projection neurons send primary axons to either the downstream premotor nucleus RA (primary motor cortex) or Area X (basal ganglia), which play important roles in song production or song learning, respectively. In addition to these long-range outputs, HVC neurons also send local axon collaterals throughout that nucleus. Despite their implications for a range of circuit models, these local processes have never been completely reconstructed. Here we use in vivo single-neuron Neurobiotin fills to examine 40 projection neurons across 31 birds with somatic positions distributed across HVC. We show that HVC(RA)and HVC(X)neurons have categorically distinct dendritic fields. Additionally, these cell classes send axon collaterals that are either restricted to a small portion of HVC ("local neurons") or broadly distributed throughout the entire nucleus ("broadcast neurons"). Overall, these processes within HVC offer a structural basis for significant local processing underlying behaviorally-relevant population activity.
PMCID:6070301
PMID: 29577283
ISSN: 1096-9861
CID: 3011222

Stable Sequential Activity Underlying the Maintenance of a Precisely Executed Skilled Behavior

Katlowitz, Kalman A; Picardo, Michel A; Long, Michael A
A vast array of motor skills can be maintained throughout life. Do these behaviors require stability of individual neuron tuning or can the output of a given circuit remain constant despite fluctuations in single cells? This question is difficult to address due to the variability inherent in most motor actions studied in the laboratory. A notable exception, however, is the courtship song of the adult zebra finch, which is a learned, highly precise motor act mediated by orderly dynamics within premotor neurons of the forebrain. By longitudinally tracking the activity of excitatory projection neurons during singing using two-photon calcium imaging, we find that both the number and the precise timing of song-related spiking events remain nearly identical over the span of several weeks to months. These findings demonstrate that learned, complex behaviors can be stabilized by maintaining precise and invariant tuning at the level of single neurons.
PMCID:6094941
PMID: 29861283
ISSN: 1097-4199
CID: 3144292

Corrigendum: A viral strategy for targeting and manipulating interneurons across vertebrate species

Dimidschstein, Jordane; Chen, Qian; Tremblay, Robin; Rogers, Stephanie L; Saldi, Giuseppe-Antonio; Guo, Lihua; Xu, Qing; Liu, Runpeng; Lu, Congyi; Chu, Jianhua; Avery, Michael C; Rashid, Mohammad S; Baek, Myungin; Jacob, Amanda L; Smith, Gordon B; Wilson, Daniel E; Kosche, Georg; Kruglikov, Illya; Rusielewicz, Tomasz; Kotak, Vibhakar C; Mowery, Todd M; Anderson, Stewart A; Callaway, Edward M; Dasen, Jeremy S; Fitzpatrick, David; Fossati, Valentina; Long, Michael A; Noggle, Scott; Reynolds, John H; Sanes, Dan H; Rudy, Bernardo; Feng, Guoping; Fishell, Gord
PMID: 28653691
ISSN: 1546-1726
CID: 2782702

Addendum: A viral strategy for targeting and manipulating interneurons across vertebrate species

Dimidschstein, Jordane; Chen, Qian; Tremblay, Robin; Rogers, Stephanie L; Saldi, Giuseppe-Antonio; Guo, Lihua; Xu, Qing; Liu, Runpeng; Lu, Congyi; Chu, Jianhua; Avery, Michael C; Rashid, Mohammad S; Baek, Myungin; Jacob, Amanda L; Smith, Gordon B; Wilson, Daniel E; Kosche, Georg; Kruglikov, Illya; Rusielewicz, Tomasz; Kotak, Vibhakar C; Mowery, Todd M; Anderson, Stewart A; Callaway, Edward M; Dasen, Jeremy S; Fitzpatrick, David; Fossati, Valentina; Long, Michael A; Noggle, Scott; Reynolds, John H; Sanes, Dan H; Rudy, Bernardo; Feng, Guoping; Fishell, Gord
PMID: 28653689
ISSN: 1546-1726
CID: 3074092

Ready, Steady, Go! Imaging Cortical Activity during Movement Planning and Execution

Banerjee, Arkarup; Long, Michael A
In this issue of Neuron, Chen et al. (2017) examine premotor activity representing motor planning, Allen et al. (2017) observe the global representation of goal-directed movement on the cortical network, and Makino et al. (2017) track changes in such dynamics throughout learning.
PMID: 28521122
ISSN: 1097-4199
CID: 2562992