Advertisement

Insights on Vision Derived from Studying Human Single Neurons

  • Jan Kamiński
  • Ueli Rutishauser
Chapter
Part of the Cognitive Science and Technology book series (CSAT)

Abstract

Investigating the living brain, and in particular relating its activity to behavior is one of the most important challenges in neuroscience. Researchers use many different techniques to explore this relationship. Careful observation of patients with brain lesions or neuroimaging methods such as functional magnetic resonance imaging (fMRI), electroencephalography (EEG), or near infra-red spectroscopy (NIRS) are examples of procedures which allow researchers to make inferences about brain activity in a non-invasive way.

Keywords

Firing Rate Entorhinal Cortex Medial Temporal Lobe Drug Resistant Epilepsy Parahippocampal Cortex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Adolphs R, Gosselin F, Buchanan TW, Tranel D, Schyns P, Damasio AR (2005) A mechanism for impaired fear recognition after amygdala damage. Nature 433:68–72CrossRefGoogle Scholar
  2. Adolphs R, Kawasaki H, Tudusciuc O, Howard MA, Heller AC, Sutherling WW, Philpott L, Ross IB, Mamelak AN, Rutishauser U (2014) Electrophysiological responses to faces in the human amygdala. In: Fried I, Rutishauser U, Cref U, Kreiman G (eds) Single neuron studies of the human brain. MIT Press, Boston, pp 229–247Google Scholar
  3. Adolphs R, Tranel D, Damasio H, Damasio A (1994) Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372:669–672CrossRefGoogle Scholar
  4. Barlow HB (2009) Single units and sensation: a neuron doctrine for perceptual psychology? Perception 38:371–394CrossRefGoogle Scholar
  5. Bettus G, Ranjeva JP, Wendling F, Bénar CG, Confort-Gouny S, Régis J, Chauvel P, Cozzone PJ, Lemieux L, Bartolomei F, Guye M (2011) Interictal functional connectivity of human epileptic networks assessed by intracerebral EEG and BOLD signal fluctuations. PLoS ONE 6:e20071CrossRefGoogle Scholar
  6. Biederman I, Bederman I (1987) Recognition-by-components: a theory of human image understanding. Psychol Rev 94:115–147CrossRefGoogle Scholar
  7. Cerf M, Thiruvengadam N, Mormann F, Kraskov A, Quiroga RQ, Koch C, Fried I (2010) On-line, voluntary control of human temporal lobe neurons. Nature 467:1104–1108CrossRefGoogle Scholar
  8. Decharms R, Zador A (2000) Neural representation and the cortical code. Annu Rev Neurosci:613–647Google Scholar
  9. Ekman P, Friesen WV (1976) Pictures of Facial Affect. Consulting Psychologists Press, Palo Alto, CAGoogle Scholar
  10. Engel J, Kuhl DE, Phelps ME, Mazziotta JC (1982) Interictal cerebral glucose metabolism in partial epilepsy and its relation to EEG changes. Ann Neurol 12:510–517CrossRefGoogle Scholar
  11. Fried I, MacDonald KA, Wilson CL (1997) Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron 18:753–765Google Scholar
  12. Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I (2008) Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322:96–101CrossRefGoogle Scholar
  13. Grill-Spector K, Malach R (2004) The human visual cortex. Annu Rev Neurosci 27:649–677CrossRefGoogle Scholar
  14. Gross CG (1994) How inferior temporal cortex became a visual area. Cereb Cortex 4:455–469CrossRefGoogle Scholar
  15. Gross CG (2002) Genealogy of the “grandmother cell”. Neuroscientist 8:512–518CrossRefGoogle Scholar
  16. Hanes DP, Thompson KG, Schall JD (1995) Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis. Exp Brain Res 103:85–96CrossRefGoogle Scholar
  17. Harding AJ, Halliday GM, Kril JJ (1998) Variation in hippocampal neuron number with age and brain volume 8:710–718Google Scholar
  18. Henze DA, Borhegyi Z, Csicsvari J, Mamiya A, Harris KD, Buzsáki G (2000) Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J Neurophysiol 84:390–400Google Scholar
  19. Hubel D, Wiesel T (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol:106–154Google Scholar
  20. Ison M, Quiroga R (2008) Selectivity and invariance for visual object perception. Front Biosci:4889–4903Google Scholar
  21. Ison MJ, Mormann F, Cerf M, Koch C, Fried I, Quiroga RQ (2011) Selectivity of pyramidal cells and interneurons in the human medial temporal lobe. J Neurophysiol 106:1713–1721CrossRefGoogle Scholar
  22. Kawasaki H, Adolphs R, Oya H, Kovach C, Damasio H, Kaufman O, Howard M (2005) Analysis of single-unit responses to emotional scenes in human ventromedial prefrontal cortex. J Cogn Neurosci 17:1509–1518CrossRefGoogle Scholar
  23. Kim S-G, Ogawa S (2012) Biophysical and physiological origins of blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab 32:1188–1206CrossRefGoogle Scholar
  24. Konorski J (1967) Integrative activity of the brain; an interdisciplinary approach. Chicago University, ChicagoGoogle Scholar
  25. Kreiman G, Fried I, Koch C (2002) Single-neuron correlates of subjective vision in the human medial temporal lobe. Proc Natl Acad Sci USA 99:8378–8383CrossRefGoogle Scholar
  26. Kreiman G, Hung CP, Kraskov A, Quiroga RQ, Poggio T, DiCarlo JJ (2006) Object selectivity of local field potentials and spikes in the macaque inferior temporal cortex. Neuron 49:433–445CrossRefGoogle Scholar
  27. Kreiman G, Koch C, Fried I (2000a) Category-specific visual responses of single neurons in the human medial temporal lobe. Nat Neurosci 3:946–953CrossRefGoogle Scholar
  28. Kreiman G, Koch C, Fried I (2000b) Imagery neurons in the human brain. Nature 408:357–361CrossRefGoogle Scholar
  29. Leonard CM, Rolls ET, Wilson FAW, Baylis GC (1985) Neurons in the amygdala of the monkey with responses selective for faces. Behav Brain Res 15:159–176CrossRefGoogle Scholar
  30. Lisman JE, Otmakhova NA (2001) Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 11:551–568CrossRefGoogle Scholar
  31. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157CrossRefGoogle Scholar
  32. Logothetis NK, Sheinberg DL (1996) Visual object recognition. Annu Rev Neurosci 19:577–621CrossRefGoogle Scholar
  33. Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735–769CrossRefGoogle Scholar
  34. Milner B, Corkin S, Teuber H-L (1968) Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. Neuropsychologia 6:215–234CrossRefGoogle Scholar
  35. Miyashita Y, Rolls ET, Cahusac PM, Niki H, Feigenbaum JD (1989) Activity of hippocampal formation neurons in the monkey related to a conditional spatial response task. J Neurophysiol 61:669–678Google Scholar
  36. Mormann F, Dubois J, Kornblith S, Milosavljevic M, Cerf M, Ison M, Tsuchiya N, Kraskov A, Quiroga RQ, Adolphs R, Fried I, Koch C (2011) A category-specific response to animals in the right human amygdala. Nat Neurosci 14:1247–1249CrossRefGoogle Scholar
  37. Mormann F, Kornblith S, Quiroga RQ, Kraskov A, Cerf M, Fried I, Koch C (2008) Latency and selectivity of single neurons indicate hierarchical processing in the human medial temporal lobe. J Neurosci 28:8865–8872CrossRefGoogle Scholar
  38. Mosher CP, Zimmerman PE, Gothard KM (2014) Neurons in the monkey amygdala detect eye contact during naturalistic social interactions. Curr Biol 24:2459–2464CrossRefGoogle Scholar
  39. Mukamel R, Ekstrom AD, Kaplan J, Iacoboni M, Fried I (2010) Single-neuron responses in humans during execution and observation of actions. Curr Biol 20:750–756CrossRefGoogle Scholar
  40. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University PressGoogle Scholar
  41. Olshausen BA, Field DJ (2004) Sparse coding of sensory inputs. Curr Opin Neurobiol 14:481–487Google Scholar
  42. Quian Quiroga R (2012) Concept cells: the building blocks of declarative memory functions. Nat Rev Neurosci 13:587–597Google Scholar
  43. Quian Quiroga R (2013) Gnostic cells in the 21st century. Acta Neurobiol Exp (Wars) 73:463–471Google Scholar
  44. Quian Quiroga R, Kraskov A, Koch C, Fried I (2009) Explicit encoding of multimodal percepts by single neurons in the human brain. Curr Biol 19:1308–1313CrossRefGoogle Scholar
  45. Quian Quiroga R, Kreiman G, Koch C, Fried I (2008) Sparse but not “grandmother-cell” coding in the medial temporal lobe. Trends Cogn Sci 12:87–91CrossRefGoogle Scholar
  46. Quian Quiroga R, Reddy L, Koch C, Fried I (2007) Decoding visual inputs from multiple neurons in the human temporal lobe. J Neurophysiol 98:1997–2007CrossRefGoogle Scholar
  47. Quian Quiroga R, Reddy L, Kreiman G, Koch C, Fried I (2005) Invariant visual representation by single neurons in the human brain. Nature 435:1102–1107CrossRefGoogle Scholar
  48. Quian Quiroga R, Kraskov A, Mormann F, Fried I, Koch C (2014) Single-cell responses to face adaptation in the human medial temporal lobe. Neuron 84:363–369CrossRefGoogle Scholar
  49. Rutishauser U, Mamelak AN, Schuman EM (2006) Single-trial learning of novel stimuli by individual neurons of the human hippocampus-amygdala complex. Neuron 49:805–813CrossRefGoogle Scholar
  50. Rutishauser U, Ross IB, Mamelak AN, Schuman EM (2010) Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464:903–907CrossRefGoogle Scholar
  51. Rutishauser U, Schuman EM, Mamelak A (2014) Single neuron correlates of declarative memory formation and retrieval in the human medial temporal lobe. In: Fried I, Rutishauser U, Cref U, Kreiman G (eds) Single neuron studies of the human brain. MIT Press, BostonGoogle Scholar
  52. Rutishauser U, Schuman EM, Mamelak AN (2008) Activity of human hippocampal and amygdala neurons during retrieval of declarative memories. Proc Natl Acad Sci USA 105:329–334CrossRefGoogle Scholar
  53. Rutishauser U, Ye S, Koroma M, Tudusciuc O, Ross IB, Chung JM, Mamelak AN (2015) Representation of retrieval confidence by single neurons in the human medial temporal lobe. Nat Neurosci 18:1–12Google Scholar
  54. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Buonocore MH, Lammers CR, Reiss AL, Amaral DG (2004) The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neurosci 24:6392–6401CrossRefGoogle Scholar
  55. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21CrossRefGoogle Scholar
  56. Sheinberg DL, Logothetis NK (1997) The role of temporal cortical areas in perceptual organization. Proc Natl Acad Sci USA 94:3408–3413CrossRefGoogle Scholar
  57. Shou T, Ruan D, Zhou Y (1986) The orientation bias of LGN neurons shows topographic relation to area centralis in the cat retina. Exp Brain Res 64:233–236CrossRefGoogle Scholar
  58. Simons DJ, Woolsey TA (1979) Functional organization in mouse barrel cortex. Brain Res 165:327–332CrossRefGoogle Scholar
  59. Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306CrossRefGoogle Scholar
  60. Sugase Y, Yamane S, Ueno S, Kawano K (1999) Global and fine information coded by single neurons in the temporal visual cortex. Nature 400:869–873CrossRefGoogle Scholar
  61. Suzuki WA (1996) Neuroanatomy of the monkey entorhinal, perirhinal and parahippocampal cortices: organization of cortical inputs and interconnections with amygdala and striatum. Semin Neurosci 8:3–12CrossRefGoogle Scholar
  62. Suzuki WA, Amaral DG (1994) Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J Comp Neurol 350:497–533CrossRefGoogle Scholar
  63. Talavage TM, Ledden PJ, Benson RR, Rosen BR, Melcher JR (2000) Frequency-dependent responses exhibited by multiple regions in human auditory cortex. Hear Res 150:225–244CrossRefGoogle Scholar
  64. Tanaka K (1996) Inferotemporal cortex and object vision. Annu Rev Neurosci 19:109–139CrossRefGoogle Scholar
  65. Tranel D, Hyman BT (1990) Neuropsychological correlates of bilateral amygdala damage. Arch Neurol 47:349–355CrossRefGoogle Scholar
  66. Tsao DY, Schweers N, Moeller S, Freiwald WA (2008) Patches of face-selective cortex in the macaque frontal lobe. Nat Neurosci 11:877–879Google Scholar
  67. Viskontas IV, Quiroga RQ, Fried I (2009) Human medial temporal lobe neurons respond preferentially to personally relevant images. Proc Natl Acad Sci USA 106:21329–21334CrossRefGoogle Scholar
  68. Wang S, Tudusciuc O, Mamelak AN, Ross IB, Adolphs R, Rutishauser U (2014) Neurons in the human amygdala selective for perceived emotion. Proc Natl Acad Sci USA 111:E3110–E3119CrossRefGoogle Scholar
  69. Waydo S, Kraskov A, Quian Quiroga R, Fried I, Koch C (2006) Sparse representation in the human medial temporal lobe. J Neurosci 26:10232–10234CrossRefGoogle Scholar
  70. Wolfe JM (1984) Reversing ocular dominance and suppression in a single flash. Vision Res 24:471–478CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Singapore 2017

Authors and Affiliations

  1. 1.Department of NeurosurgeryCedars-Sinai Medical CenterPasadenaUSA
  2. 2.Division of Biology and Biological EngineeringCalifornia Institute of TechnologyPasadenaUSA

Personalised recommendations