48
49
showing that area F4 hosts neurons with somatosensory and visual response properties (e.g., Graziano et al. 1994; Fogassi et al., 1996). Indeed, the recorded neurons discharge to the tactile stimulation of the face, forelimbs or trunk; they also responded during visual stimulations, up to 70 cm. The firing rate maps show that the neural activity changes gradually along the three spatial dimensions, as emerged from other studies (e.g., Graziano et al., 1997a; Duhamel et al.
1998).
We next examined how the recorded neurons might form a population-level representation of visuo-tactile stimulations. Thanks to a decoding model, it is sought to predict stimulus properties (in this case its position) with a linear combination of neural responses. For instance, the neural decoding finds considerable applications in Brain Machine Interface, like neural prosthesis (Hatsopoulos & Donoghue, 2009). Our results suggest that neural ensembles encode object positions both during tactile stimulations and during visual stimulations. A better accuracy seems to be achieved in the decoding of tactile stimuli, particularly when the stimulation occurs along z axis. Concerning the visual condition, it appears more difficult to predict the stimuli position in the course of the whole stimulations instead of during a single type of stimulation, likely due to a wider range of possible movements. It is not completely clear which kind of visual stimulations yield the best decoding accuracy, but increasing the data set may certainly help to get more precise and reliable results. We observed a greater ability to predict the object position along the horizontal axis, in agreement with previous studies emphasizing that “the terrestrial life needs more horizontal scanning than vertical scanning”
(Kobayashi & Kohshima, 2001).
50
macaque premotor cortex. Only single-units are considered, but next steps may consider to use multi-unit activity as well. It could also be interesting to compare the tactile and the visual properties of each single and multi-unit, examining a possible visuo-tactile matching, as reported by previous studies (Fogassi et al., 1996). Furthermore, control conditions could be added, in order to avoid confounding factors associated with the nature of the object used for the stimulation or the type of stimulation applied (e.g. by placing a different object at the end of the stick).
The apparatus employed in this study reflects classical laboratory settings (for example, the use of a primate chair). However, the findings obtained in this setting can be compared with those collected on the same neurons recorded during freely behaving sessions in which the monkey move spontaneously and actively during active exploration of the environment (Bonini, 2019), thereby increasing the ecological validity of the findings and comparing passive stimulations with active changes in the body-object positions because of monkey’s active movement.
The values of PPS fields likely correspond with the relevance of potential motor actions in relation to the stimuli (Bufacchi and Iannetti 2018), suggesting that “contact-related behavioural relevance” refers to the perspective of interactive behaviour: according to this theoretical framework, “interaction with the environment involves continuous and simultaneous processes of sensorimotor control and action selection from among the distributed representations of a limited number of response options” (Cisek & Kalaska, 2010). The parietal and premotor cortices – the cortical regions thought to underlie the peripersonal space representation – appear to take on great relevance the potential actions’ specification (e.g.,
51
revealed in constrained behavioural conditions may apply or work in a different way during unconstrained, active interactions of a subject with its physical and social environment.
52
REFERENCES
Aimola, L., Schindler, I., & Venneri, A. (2013). Task- and response related dissociations between neglect in near and far space: A morphometric case study. Behavioural Neurology, 27(3), 245-257. doi:10.3233/BEN-2012-110243
Avillac, M., Ben Hamed, S., & Duhamel, J. R. (2007). Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey. The Journal of Neuroscience, 27(8), 1922-1932. doi:10.1523/JNEUROSCI.2646-06.2007
Bassolino, M., Serino, A., Ubaldi, S., & Làdavas, E. (2010). Everyday use of the computer mouse extends peripersonal space representation. Neuropsychologia, 48, 803-811.
doi:10.1016/j.neuropsychologia.2009.11.009
Beck, B. B. (1980). Animal Tool Behavior: The use and manufacture of tool. New York:
Garland Press.
Berti, A., & Frassinetti, F. (2000). When Far Becomes Near: Remapping of Space by Tool Use.
Journal of Cognitive Neuroscience, 12(3), 415-420. doi:10.1162/089892900562237 Bonini, L. (2019). Refinement techniques in non-human primate neuroscientific research. Ann
Ist Super Sanità, 55(4), 408-412. doi:10.4415/ANN_19_04_18
Bonini, L., Maranesi, M., Livi, A., Fogassi, L., & Rizzolatti, G. (2014). Space-Dependent Representation of Objects and Other’s Action in Monkey Ventral Premotor Grasping Neurons. The Journal of Neuroscience, 34(11), 4108-4119.
doi:10.1523/JNEUROSCI.4187-13.2014
Brain, W. R. (1941). Visual disorientation with special referene to lesions of the right cerebral hemisphere. Brain, 64, 244-272.
Bremmer, F., Duhamel, J. R., & Graf, W. (2002). Heading encoding in the macaque ventral intraparietal area (VIP). European Journal of Neuroscience, 16, 1554-1568.
doi:10.1046/j.1460-9568.2002.02207.x
Brozzoli, C., Gentile, G., Bergouignan, L., & Ehrsson, H. H. (2013). A Shared Representation of the Space Near Oneself and Others in the Human Premotor Cortex. Current Biology, 23, 1764-1768. doi:10.1016/j.cub.2013.07.004
Bruni, S., Giorgetti, V., Bonini, L., & Fogassi, L. (2015). Processing and Integration of Contextual Information in Monkey Ventrolateral Prefrontal Neurons during Selection and Execution of Goal-Directed Manipulative Actions. The Journal of Neuroscience, 35(34), 11877–11890. doi:10.1523/JNEUROSCI.1938-15.2015
53
in Cognitive Sciences, 22(12), 1076-1090. doi:10.1016/j.tics.2018.09.004
Caggiano, V., Fogassi, L., Rizzolatti, G., Thier, P., & Casile, A. (2009). Mirror Neurons Differentially Encode the Peripersonal and Extrapersonal Space of Monkeys. Science, 324(403), 403-406. doi:10.1126/science.1166818
Canzoneri, E., Marzolla, M., Amoresano, A., Verni, G., & Serino, A. (2013). Amputation and prosthesis implantation shape body and peripersonal space representations. Scientific Reports, 3, 2844. doi:10.1038/srep02844
Chen, A., DeAngelis, G. C., & Angelaki, D. E. (2011). Representation of Vestibular and Visual Cues to Self-Motion in Ventral Intraparietal Cortex. The Journal of Neuroscience, 31(33), 12036 –12052. doi:10.1523/JNEUROSCI.0395-11.2011
Chen, A., Gu, Y., Liu, S., DeAngelis, G. C., & Angelaki, D. E. (2016). Evidence for a Causal Contribution of Macaque Vestibular, But Not Intraparietal, Cortex to Heading Perception. The Journal of Neuroscience, 36(13), 3789–3798.
doi:10.1523/JNEUROSCI.2485-15.2016
Chung, J. E., Magland, , J. F., Barnett, A. H., Tolosa, V. M., Tooker, A. C., Lee, K. Y., . . . Greengard, L. F. (2017). A Fully Automated Approach to Spike Sorting. Neuron, 95(6), 381–1394. doi:10.1016/j.neuron.2017.08.030
Cisek, P., & Kalaska, J. F. (2010). Neural Mechanisms for Interacting with a World Full of
Action Choices. Annu. Rev. Neurosci, 33, 269-298.
doi:10.1146/annurev.neuro.051508.135409
Cléry , J., Guipponi, O., Wardak, C., & Ben Hammed, S. (2015). Neuronal bases of peripersonal and extrapersonal spaces, their plasticity and their dynamics: Knowns and unknowns.
Neuropsychologia, 70, 313-326. doi:10.1016/j.neuropsychologia.2014.10.022
Colby, C. L., Duhamel, J. R., & Goldberg, M. E. (1993). Ventral intraparietal area of the macaque: anatomic location and visual response properties. Journal of Neurophysiology, 69(3), 902-914. doi:10.1152/jn.1993.69.3.902
Cowey, A., Small, M., & Ellis, S. (1994). Left visuo-spatial neglect can be worse in far than in near space. Neuropsychologia, 32(9), 1059-1066. doi:10.1016/0028-3932(94)90152-X de Vignemont, F., & Iannetti, G. (2015). How many peripersonal space? Neuropsychologia,
70, 327-334. doi:10.1016/j.neuropsychologia.2014.11.018
di Pellegrino, G., & Làdavas, E. (2015). Peripersonal space in the brain. Neuropsychologia, 66, 126-133. doi:10.1016/j.neuropsychologia.2014.11.011
di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: a neurophysiological study. Experimental Brain Research, 91(1), 176-180. doi:10.1007/BF00230027
54
receptive fields in parietal cortex neurons. Nature, 389(6653), 845-848.
doi:10.1038/39865
Duhamel, J. R., Colby, C. L., & Goldberg, M. E. (1998). Ventral Intraparietal Area of the Macaque: Congruent Visual and Somatic Response Properties. Journal of Neurophysiology, 79(1), 126-136. doi:10.1152/jn.1998.79.1.126
Fogassi, L., Gallese, V., Fadiga, L., Luppino, G., Matelli, M., & Rizzolatti, G. (1996). Coding of Peripersonal Space in Inferior Premotor Cortex (Area F4). Journal of Neurophysiology, 76(1), 141-157. doi:10.1152/jn.1996.76.1.141
Friard, O., & Gamba, M. (2016). BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods in Ecology and Evolution, 7, 1325-1330. doi:10.1111/2041-210X.12584
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119, 593-609. doi: 10.1093/brain/119.2.593
Gentilucci, M., Fogassi, L., Luppino, G., Matelli, M., Camarda, R., & Rizzolatti, G. (1988).
Functional organization of inferior area 6 in the macaque monkey. Experimental Brain Research, 71(3), 475-490. doi:10.1007/BF00248741
Gentilucci, M., Scandolara, C., Pigarev, I. N., & Rizzolatti, G. (1983). Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position.
Experimental Brain Research, 50(2-3), 464-468. doi:10.1007/BF00239214
Graziano, M. A., Alisharan, S. E., Hu, X., & Gross, C. G. (2002). The clothing effect: Tactile neurons in the precentral gyrus do not respond to the touch of the familiar primate chair.
PNAS, 99(18), 11930–11933. doi:10.1073/pnas.172380399
Graziano, M. S. (1999). Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. Proc. Natl. Acad. Sci., 96(18), 10418-10421.
doi:10.1073/pnas.96.18.10418
Graziano, M. S. (2006). The Organization of Behavioral Repertoire in Motor Cortex. Annual Review of Neuroscience, 29, 105-134. doi:10.1146/annurev.neuro.29.051605.112924 Graziano, M. S., & Gross, C. G. (1993). A bimodal map of space: somatosenory fields in the
macaque putamen with corresponding visual receptive fields. Experimental Brain Research, 97(1), 96-109. doi:10.1007/BF00228820
Graziano, M. S., & Gross, C. G. (1995). The representation of extrapersonal space: A possible role for bimodal, visual-tactile neurons. In M. S. Gazzaniga, The Cognitive Neuroscience (p. 1021-1034). Cambridge (MA): MIT Press.
Graziano, M. S., Aflalo, T. N., & Cooke, D. F. (2005). Arm Movements Evoked by Electrical Stimulation in the Motor Cortex of Monkeys. Journal of Neurophysiology, 94(6), 4209-4223. doi:10.1152/jn.01303.2004
55
Cortex. Journal of Neurophysiology, 77(5), 2268-2292. doi:10.1152/jn.1997.77.5.2268 Graziano, M. S., Hu, X. T., & Gross, C. G. (1997b). Coding the Locations of Objects in the
Dark. Science, 277(5323), 239-241. doi:10.1126/science.277.5323.239
Graziano, M. S., Reiss, L. A., & Gross, C. G. (1999). Neuronal representation of the location of nearby sounds. Nature, 397(6718), 428-430. doi:10.1038/17115
Graziano, M. S., Yap, G. S., & Gross, C. G. (1994). Coding of Visual Space by Premotor Neurons. Science, 266(5187), 1054-1057. doi:10.1126/science.7973661
Grieves, R. M., Jedidi-Ayoub, S., Mishchanchuk, K., Liu, A., Renaudineau, S., & Jeffrey, K. J.
(2020). The place-cell representation of volumetric space in rats. Nature Communication, 11(1), 789. doi:10.1038/s41467-020-14611-7
Halligan, P. W., & Marshall, J. C. (1991). Left neglect for near but not far space in man. Nature, 350(6318), 498-500. doi:10.1038/350498a0
Hatsopoulos, N. G., & Donoghue, J. P. (2009). The Science of Neural Interface Systems. Annu Rev Neurosci., 32, 249-266. doi:10.1146/annurev.neuro.051508.135241.
Hediger, H. (1950). Wild Animals in Captivity. Buttersworth Scientific Publications.
Hediger, H. (1955). Studies of the psychology and behavior of captive animals in zoos and circuses. London: Butterworths Scientific Publications.
Heed, T., Habets, B., Sebanz, N., & Knoblich, G. (2010). Others’ Actions Reduce Crossmodal Integration in Peripersonal Space. Current Biology, 20(15), 1345–1349.
doi:10.1016/j.cub.2010.05.068
Hunley, S. B., & Lourenco, S. F. (2018). What is peripersonal space? An examination of unresolved empirical issues and emerging findings. WIREs Cognitive Science, 9, :e1472. doi:10.1002/wcs.1472
Hurley, S. (1998). Consciousness in action. Cambridge, MA: Harvard University Press.
Hyvarinen, J. (1981). Regional distribution of functions in parietal association area 7 of the monkey. Brain Research, 206(2), 287-303. doi:10.1016/0006-8993(81)90533-3
Iriki, A., Tanaka, M., & Iwamura, Y. (1996). Coding of modified body schema during tool use by macacque poscentral neurones. Neuroreport, 7(14), 2325–2330. doi:
10.1097/00001756-199610020-00010
Ishida, H., Nakajima, K., Inase, M., & Murata, A. (2010). Shared Mapping of Own and Others' Bodies in Visuotactile Bimodal Area of Monkey Parietal Cortex. Journal of Cognitive Neuroscience, 22(1), 83-96. doi:10.1162/jocn.2009.21185
Kobayashi, H., & Kohshima, S. (2001). Unique morphology of the human eye and its adaptive meaning: Comparative studies on external morphology of the primate eye. Journal of Human Evolution, 40(5), 419-435. doi:10.1006/jhev.2001.0468
56
neurons in lateral part of associative area 7 in awake monkeys. Experimental Brain Research, 34(2), 299-320. doi:10.1007/BF00235675
Maranesi, M., Livi, A., & Bonini, L. (2017). Spatial and viewpoint selectivity for others’
observed actions in monkey ventral premotor mirror neurons. Scientific Reports, 7(1), 8231. doi:10.1038/s41598-017-08956-1
Maravita, A., & Iriki, A. (2004). Tools for the body (schema). Trends in Cognitive Sciences, 8(2), 79-86. doi:10.1016/j.tics.2003.12.008
Matelli, M., Camarda, R., Glickstein, M., & Rizzolatti, G. (1986). Afferent and efferent projections of the inferior area 6 in the macaque monkey. Journal of Comparative Neurology, 251(3), 281-298. doi:10.1002/cne.902510302
Matelli, M., Luppino, G., & Rizzolatti, G. (1985). Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behavioural Brain Research, 18(2), 125-136. doi:10.1016/0166-4328(85)90068-3
McCabe, K. A., Rassenti, S. J., & Smith, V. L. (1996). Game theory and reciprocity in some extensive form experimental games. PNAS, 93(23), 13421–13428,.
doi:10.1073/pnas.93.23.13421
Merleau-Ponty, M. (1962). Phenomenology of Perception. (C. Smith, Trad.) London, UK:
Routledge and Kegan Paul.
O'Keefe, J., & Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Research, 34(1), 171-175.
doi:10.1016/0006-8993(71)90358-1
Penfield, W., & Boldrey, E. (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain, 60(4), 389-443.
doi:10.1093/brain/60.4.389
Phillips, K. A., Bales, K. L., Capitanio, J. P., Conley, A., Czoty, P. W., 't Hart, B. A., . . . Voytko, M. L. (2014). Why Primate Models Matter. American Journal of Primatology, 76(9), 801-827. doi:10.1002/ajp.22281
Piaget, J. (1952). The Origins of Intelligence in Children. New York: International Universities Press.
Rizzolatti, G., & Luppino, G. (2001). The Cortical Motor System. Neuron, 31(6), 889-901.
doi:10.1016/s0896-6273(01)00423-8
Rizzolatti, G., & Sinigaglia, C. (2006). So quel che fai. Il cervello che agisce e i neuroni specchio. Milano: Raffaello Cortina Editore.
Rizzolatti, G., Matelli, M., & Pavesi, G. (1983). Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys.
Brain, 106, 655–673. doi:10.1093/brain/106.3.655
57
periarcuate neurons in macaque monkeys. II. Visual responses. Behavioural Brain Research, 2(2), 147-163. doi:10.1016/0166-4328(81)90053-x
Rozzi, S., Ferrari, P. F., Bonini, L., Rizzolatti, G., & Fogassi, L. (2008). Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. European Journal of Neuroscience, 28, 1569–1588.
doi:10.1111/j.1460-9568.2008.06395.x
Sambo, C. F., & Iannetti, G. D. (2013). Better Safe Than Sorry? The Safety Margin Surrounding the Body Is Increased by Anxiety. The Journal of Neuroscience, 33(35), 14225–14230.
doi:10.1523/JNEUROSCI.0706-13.2013
Schlack, A., Sterbing-D’Angelo, S. J., Hartung, K., Hoffmann, K. P., & Bremmer, F. (2005).
Multisensory Space Representations in the Macaque Ventral Intraparietal Area. The Journal of Neuroscience, 25(18), 4616-4625. doi:10.1523/JNEUROSCI.0455-05.2005 Serino, A. (2019). Peripersonal space (PPS) as a multisensory interface between the individual
and the environment, defining the space of the self. Neuroscience and Biobehavioral Reviews, 99, 138-159. doi:10.1016/j.neubiorev.2019.01.016
Serino, A., Bassolino, M., Farnè, A., & Làdavas, E. (2007). Extended Multisensory Space in Blind Cane Users. Psychological Science, 18(7), 642-648. doi:10.1111/j.1467-9280.2007.01952.x
Stachenfeld, K., Botvinick, M. M., & Gershman, S. J. (2017). The hippocampus as a predictive map. Nature Neuroscience, 20(11), 1643-1653. doi:10.1038/nn.4650
Taffou, M., & Viaud-Delmon, I. (2014). Cynophobic fear adaptively extends peri-personal space. Frontiers in Psychiatry, 5, 122. doi:10.3389/fpsyt.2014.00122
Teneggi, C., Canzoneri, E., di Pellegrino, G., & Serino, A. (2013). Social Modulation of Peripersonal Space Boundaries. Current Biology, 23(5), 406-411.
doi:10.1016/j.cub.2013.01.043
Vallar, G., & Papagno, C. (2018). Manuale di neuropsicologia. Bologna: il Mulino.
Van der Stoep, N., Nijboer, T. C., Van der Stigchel, S., & Spence, C. (2015). Multisensory interactions in the depth plan e in front and rear space: A review. Neuropsychologia, 70, 335-349. doi:10.1016/j.neuropsychologia.2014.12.007
Weiss, P. H., Marshall, J. C., Zilles, K., & Fink, G. R. (2003). Are action and perception in near and far space additive or interactive factors? NeuroImage, 18(4), 837-846.
doi:10.1016/s1053-8119(03)00018-1
Whitlock, J. R., Sutherland, R. J., Witter, M. P., Moser, M.-B., & Moser, E. I. (2008).
Navigating from hippocampus to parietal cortex. Proceedings of the National Academy of Sciences, 105(39), 14755-14762. doi:10.1073/pnas.0804216105