Secondary Somatosensory and Posterior Insular Cortices: a Somatomotor Hub for Object Prehension and Manipulation Movements

Overview

Journal Front Integr Neurosci

Date 2024 May 10

PMID 38725800

Authors

Hiroaki Ishida

Laura Clara Grandi

Luca Fornia

Affiliations

Soon will be listed here.

Abstract

The secondary somatosensory cortex (SII) and posterior insular cortex (pIC) are recognized for processing touch and movement information during hand manipulation in humans and non-human primates. However, their involvement in three-dimensional (3D) object manipulation remains unclear. To investigate neural activity related to hand manipulation in the SII/pIC, we trained two macaque monkeys to grasp three objects (a cone, a plate, and a ring) and engage in visual fixation on the object. Our results revealed that 19.4% ( = 50/257) of the task-related neurons in SII/pIC were active during hand manipulations, but did not respond to passive somatosensory stimuli. Among these neurons, 44% fired before hand-object contact (reaching to grasping neurons), 30% maintained tonic activity after contact (holding neurons), and 26% showed continuous discharge before and after contact (non-selective neurons). Object grasping-selectivity varied and was weak among these neurons, with only 24% responding to fixation of a 3D object (visuo-motor neurons). Even neurons unresponsive to passive visual stimuli showed responses to set-related activity before the onset of movement (42%, = 21/50). Our findings suggest that somatomotor integration within SII/pIC is probably integral to all prehension sequences, including reaching, grasping, and object manipulation movements. Moreover, the existence of a set-related activity within SII/pIC may play a role in directing somatomotor attention during object prehension-manipulation in the absence of vision. Overall, SII/pIC may play a role as a somatomotor hub within the lateral grasping network that supports the generation of intentional hand actions based on haptic information.

References

Raos V, Umilta M, Murata A, Fogassi L, Gallese V . Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. J Neurophysiol. 2005; 95(2):709-29. DOI: 10.1152/jn.00463.2005. View

Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou G, Matelli M . Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex. 2005; 16(10):1389-417. DOI: 10.1093/cercor/bhj076. View

Kurata K, Wise S . Premotor cortex of rhesus monkeys: set-related activity during two conditional motor tasks. Exp Brain Res. 1988; 69(2):327-43. DOI: 10.1007/BF00247578. View

Brown H, Friston K, Bestmann S . Active inference, attention, and motor preparation. Front Psychol. 2011; 2:218. PMC: 3177296. DOI: 10.3389/fpsyg.2011.00218. View

Murata A, Gallese V, Luppino G, Kaseda M, Sakata H . Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. J Neurophysiol. 2000; 83(5):2580-601. DOI: 10.1152/jn.2000.83.5.2580. View

Burton H, Sinclair R . Attending to and remembering tactile stimuli: a review of brain imaging data and single-neuron responses. J Clin Neurophysiol. 2001; 17(6):575-91. DOI: 10.1097/00004691-200011000-00004. View

Keysers C, Wicker B, Gazzola V, Anton J, Fogassi L, Gallese V . A touching sight: SII/PV activation during the observation and experience of touch. Neuron. 2004; 42(2):335-46. DOI: 10.1016/s0896-6273(04)00156-4. View

Soso M, Fetz E . Responses of identified cells in postcentral cortex of awake monkeys during comparable active and passive joint movements. J Neurophysiol. 1980; 43(4):1090-110. DOI: 10.1152/jn.1980.43.4.1090. View

Krubitzer L, Clarey J, Tweedale R, Elston G, Calford M . A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys. J Neurosci. 1995; 15(5 Pt 2):3821-39. PMC: 6578217. View

10.

Grandi L, Gerbella M . Single Neurons in the Insular Cortex of a Macaque Monkey Respond to Skin Brushing: Preliminary Data of the Possible Representation of Pleasant Touch. Front Behav Neurosci. 2016; 10:90. PMC: 4877530. DOI: 10.3389/fnbeh.2016.00090. View

11.

Murata A, Fadiga L, Fogassi L, Gallese V, Raos V, Rizzolatti G . Object representation in the ventral premotor cortex (area F5) of the monkey. J Neurophysiol. 1997; 78(4):2226-30. DOI: 10.1152/jn.1997.78.4.2226. View

12.

Hyvarinen J, Poranen A, Jokinen Y . Influence of attentive behavior on neuronal responses to vibration in primary somatosensory cortex of the monkey. J Neurophysiol. 1980; 43(4):870-82. DOI: 10.1152/jn.1980.43.4.870. View

13.

Borra E, Gerbella M, Rozzi S, Luppino G . The macaque lateral grasping network: A neural substrate for generating purposeful hand actions. Neurosci Biobehav Rev. 2017; 75:65-90. DOI: 10.1016/j.neubiorev.2017.01.017. View

14.

Hsiao S, OShaughnessy D, Johnson K . Effects of selective attention on spatial form processing in monkey primary and secondary somatosensory cortex. J Neurophysiol. 1993; 70(1):444-7. DOI: 10.1152/jn.1993.70.1.444. View

15.

Hikosaka O, Tanaka M, Sakamoto M, Iwamura Y . Deficits in manipulative behaviors induced by local injections of muscimol in the first somatosensory cortex of the conscious monkey. Brain Res. 1985; 325(1-2):375-80. DOI: 10.1016/0006-8993(85)90344-0. View

16.

Robinson C, Burton H . Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis. J Comp Neurol. 1980; 192(1):69-92. DOI: 10.1002/cne.901920105. View

17.

Bakola S, Gamberini M, Passarelli L, Fattori P, Galletti C . Cortical connections of parietal field PEc in the macaque: linking vision and somatic sensation for the control of limb action. Cereb Cortex. 2010; 20(11):2592-604. DOI: 10.1093/cercor/bhq007. View

18.

Ishida H, Fornia L, Grandi L, Umilta M, Gallese V . Somato-motor haptic processing in posterior inner perisylvian region (SII/pIC) of the macaque monkey. PLoS One. 2013; 8(7):e69931. PMC: 3728371. DOI: 10.1371/journal.pone.0069931. View

19.

Gharbawie O, Stepniewska I, Qi H, Kaas J . Multiple parietal-frontal pathways mediate grasping in macaque monkeys. J Neurosci. 2011; 31(32):11660-77. PMC: 3166522. DOI: 10.1523/JNEUROSCI.1777-11.2011. View

20.

Sakata H, Taira M, Kusunoki M, Murata A, Tanaka Y . The TINS Lecture. The parietal association cortex in depth perception and visual control of hand action. Trends Neurosci. 1997; 20(8):350-7. DOI: 10.1016/s0166-2236(97)01067-9. View