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Neurophysiology of prehension. I. Posterior parietal cortex and object-oriented hand behaviors

Gardner, Esther P; Babu, K Srinivasa; Reitzen, Shari D; Ghosh, Soumya; Brown, Alice S; Chen, Jessie; Hall, Anastasia L; Herzlinger, Michael D; Kohlenstein, Jane B; Ro, Jin Y
Hand manipulation neurons in areas 5 and 7b/anterior intraparietal area (AIP) of posterior parietal cortex were analyzed in three macaque monkeys during a trained prehension task. Digital video recordings of hand kinematics synchronized to neuronal spike trains were used to correlate firing rates of 128 neurons with hand actions as the animals grasped and lifted rectangular and round objects. We distinguished seven task stages: approach, contact, grasp, lift, hold, lower, and relax. Posterior parietal cortex (PPC) firing rates were highest during object acquisition; 88% of task-related area 5 neurons and 77% in AIP/7b fired maximally during stages 1, 2, or 3. Firing rates rose 200-500 ms before contact, peaked at contact, and declined after grasp was secured. 83% of area 5 neurons and 72% in AIP/7b showed significant increases in mean rates during approach as the fingers were preshaped for grasp. Somatosensory signals at contact provided feedback concerning the accuracy of reach and helped guide the hand to grasp sites. In error trials, tactile information was used to abort grasp, or to initiate corrective actions to achieve task goals. Firing rates declined as lift began. 41% of area 5 neurons and 38% in AIP/7b were inhibited during holding, and returned to baseline when grasp was relaxed. Anatomical connections suggest that area 5 provides somesthetic information to circuits linking AIP/7b to frontal motor areas involved in grasping. Area 5 may also participate in sensorimotor transformations coordinating reach and grasp behaviors and provide on-line feedback needed for goal-directed hand movements
PMCID:2868366
PMID: 16971679
ISSN: 0022-3077
CID: 111675

Object feature representation in posterior parietal cortex (PPC) during prehension [Meeting Abstract]

Gardner, EP; Babu, KS; Debowy, DJ; Ghosh, S; Chen, Jessie
ORIGINAL:0007460
ISSN: 1558-3635
CID: 162617

Representation of hand kinematics during prehension in posterior parietal cortex (PPC) [Meeting Abstract]

Chen, Jessie; Debowy, DJ; Babu, KS; Ghosh, S; Gardner, EP
ORIGINAL:0007461
ISSN: 1558-3635
CID: 162618

Cortical mechanisms in the control of prehension [Meeting Abstract]

Chen, Jessie; Debowy, DJ; Babu, KS; Gardner, EP
ORIGINAL:0007463
ISSN: 1558-3635
CID: 162620

Towards effective and rewarding data sharing

Gardner, Daniel; Toga, Arthur W; Ascoli, Giorgio A; Beatty, Jackson T; Brinkley, James F; Dale, Anders M; Fox, Peter T; Gardner, Esther P; George, John S; Goddard, Nigel; Harris, Kristen M; Herskovits, Edward H; Hines, Michael L; Jacobs, Gwen A; Jacobs, Russell E; Jones, Edward G; Kennedy, David N; Kimberg, Daniel Y; Mazziotta, John C; Miller, Perry L; Mori, Susumu; Mountain, David C; Reiss, Allan L; Rosen, Glenn D; Rottenberg, David A; Shepherd, Gordon M; Smalheiser, Neil R; Smith, Kenneth P; Strachan, Tom; Van Essen, David C; Williams, Robert W; Wong, Stephen T C
PMID: 15046250
ISSN: 1539-2791
CID: 138479

Sensory monitoring of prehension in the parietal lobe: a study using digital video

Gardner, Esther P; Debowy, Daniel J; Ro, Jin Y; Ghosh, Soumya; Babu, K Srinivasa
Digital video provides technological tools for monitoring hand kinematics during prehension, and for correlating motor behavior with the simultaneously recorded firing patterns of neurons in parietal cortex of monkeys. The constancy of the hand action in the task allowed us to derive population responses of neurons in both S-I and posterior parietal cortex (PPC) from serial single unit recordings. Activity of PPC neurons preceded that in S-I, and was often shape-selective for particular objects, suggesting that they play an important role in motor planning of prehension. Detailed sensory monitoring of hand-object interactions occurred in S-I, where distinct groups of neurons responded to specific behaviors such as grasping, lifting, holding or releasing objects
PMID: 12356452
ISSN: 0166-4328
CID: 39582

Comparison of neuronal firing rates in somatosensory and posterior parietal cortex during prehension

Debowy DJ; Ghosh S; Ro JY; Gardner EP
To evaluate their functional roles during prehension, single-unit recordings were made in the hand area of primary somatosensory areas 3b, 1 and 2 (S-I) and posterior parietal areas 5 and 7 (PPC) of the same animal. Response profiles of mean firing rate during performance of a multistage reach, grasp, and lift task were analyzed to determine the period(s) of peak firing and to measure statistically significant rises or falls in rate compared with baseline. We used the peak firing stage(s) to subdivide the population into classes tuned to single actions or two successive stages, or into multiaction groups that had sustained facilitation (BT) or inhibition (GI) during hand-object interactions. Four times as many neurons fired at peak rates during acquisition stages (approach, contact, grasp) than upon release, and their firing rates were higher. Grasping evoked the strongest responses, as grasp-tuned neurons had the highest peak rates in the population; BT, contact-grasp, and grasp-lift cells also fired maximally in the grasp stage. Grasping also coincided with maximal inhibition of GI cells, as well as of neurons tuned to approach or relaxation of grasp. Holding evoked the lowest mean rates, and had the fewest tuned cells. S-I and PPC showed significant differences in behaviors evoking peak firing as well as facilitation and inhibition; these correlated with input modalities in each area. Hand contact with the object and positioning of the fingers for grasp was the most strongly represented behavior in anterior S-I, where 61% received tactile inputs from glabrous skin. Nearly 60% were facilitated at contact, 38% fired at peak rates, and 10% were inhibited; release of grasp evoked peak firing in only 5% of 3b-1 neurons. In posterior S-I, where proportions of tactile and deep inputs were similar, positioning and grasping elicited peak responses in 38% and 31%, respectively; 80% were facilitated or inhibited during grasping. During lift and hold, inhibition rose to 43%, while excitation declined under 10%. PPC had the highest proportions firing at peak rates during hand preshaping before contact (28%) and had the most facilitated responses (38%) in this stage. Only 10% fired at peak rates during grasping. During later manipulatory actions, proportions of facilitated and inhibited responses in PPC were similar to those in posterior S-I. The data support models in which PPC plans hand movements during prehension rather than guiding their execution. Sensory monitoring of hand-object interaction occurs in S-I, where cells sense specific hand behaviors, signal stage completion, enable error correction, and may update grasp programs formulated in PPC. The results are discussed in relation to those obtained from lesion studies in humans
PMID: 11355375
ISSN: 0014-4819
CID: 20663

Common data model for neuroscience data and data model exchange

Gardner D; Knuth KH; Abato M; Erde SM; White T; DeBellis R; Gardner EP
OBJECTIVE: Generalizing the data models underlying two prototype neurophysiology databases, the authors describe and propose the Common Data Model (CDM) as a framework for federating a broad spectrum of disparate neuroscience information resources. DESIGN: Each component of the CDM derives from one of five superclasses-data, site, method, model, and reference-or from relations defined between them. A hierarchic attribute-value scheme for metadata enables interoperability with variable tree depth to serve specific intra- or broad inter-domain queries. To mediate data exchange between disparate systems, the authors propose a set of XML-derived schema for describing not only data sets but data models. These include biophysical description markup language (BDML), which mediates interoperability between data resources by providing a meta-description for the CDM. RESULTS: The set of superclasses potentially spans data needs of contemporary neuroscience. Data elements abstracted from neurophysiology time series and histogram data represent data sets that differ in dimension and concordance. Site elements transcend neurons to describe subcellular compartments, circuits, regions, or slices; non-neuroanatomic sites include sequences to patients. Methods and models are highly domain-dependent. CONCLUSIONS: True federation of data resources requires explicit public description, in a metalanguage, of the contents, query methods, data formats, and data models of each data resource. Any data model that can be derived from the defined superclasses is potentially conformant and interoperability can be enabled by recognition of BDML-described compatibilities. Such metadescriptions can buffer technologic changes
PMCID:134589
PMID: 11141510
ISSN: 1067-5027
CID: 26821

Depression of neuronal firing rates in somatosensory and posterior parietal cortex during object acquisition in a prehension task

Ro JY; Debowy D; Ghosh S; Gardner EP
Prehension is an object-oriented behavior consisting of four components: reach, grasp, manipulation, and release. To determine how such actions are represented in primary somatosensory (S-I) and posterior parietal cortex (PPC), we used digital video to synchronize spike trains of neurons recorded in Brodmann's areas 3b, 1, 2, 5, and 7 with the hand kinematics as monkeys performed a prehension task. Statistical analyses indicated that one-third of task-modulated neurons showed significantly depressed firing rates during object acquisition and/or manipulation. This population was dominated by neurons innervated by deep receptors that sensed extension movements of the fingers, or by tactile receptors in hairy skin sensing stretch. Grasp-inhibited responses were the most common type. Tonic firing rates of these cells dropped significantly during approach as the hand was preshaped for grasping, or at contact when grasp was initiated, and persisted until hand motion ceased or as the grip relaxed. Maximum suppression of firing occurred at grasp completion. Their lack of specificity for particular hand behaviors formed the inhibitory counterpart of broadly tuned cells that fired prolonged bursts during grasp and manipulatory stages of prehension. The remainder of the task-inhibited population showed biphasic responses. Firing rates were significantly depressed during grasping and manipulation when the hand interacted directly with the object, but were enhanced prior to contact, when the hand was preshaped (approach-tuned), or upon relaxation of grasp and release of the object from the hand (loweror relax-tuned). Grasp-inhibited responses occurred primarily in S-I, whereas biphasic inhibitory activity was recorded mainly in PPC. Suppression of activity within these populations may thereby increase the saliency of excitatory responses to acquisition and manipulation of objects. Reduction of firing during prehension might also signal the flexed postures used to retain objects in the hand, rather than a generalized gating of sensory information. The similarity of responses to active and passive extension movements suggests that the inhibitory responses may provide important postural and motor information about the hand kinematics when performing skilled tasks
PMID: 11104122
ISSN: 0014-4819
CID: 39506

Posterior parietal cortex (PPC) may initiate goal-directed actions of the hand [Meeting Abstract]

Gardner, E P; Debowy, D; Ro, J Y; Ghosh, S
BIOSIS:200000148691
ISSN: 0190-5295
CID: 15836