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Cognitively Relevant Recoding in Hippocampus: Beneficial Feedback of Ensemble Codes in a Closed Loop Paradigm

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Electrophysiological Recording Techniques

Part of the book series: Neuromethods ((NM,volume 54))

Abstract

The use of population codes derived from ensembles of rat hippocampal neurons to control performance of a delayed-nonmatch-to-sample (DNMS) memory task illustrates the important functional and organizational specificity of simultaneously active neurons in this important brain region. In this chapter, we show that online population analyses of firing patterns of 15–35 hippocampal neurons in a single trial provides an ensemble representation (i.e. code) of Sample response information sufficient for utilization, after an imposed (1–30 s) delay interval, to make the required Nonmatch decision on the same trial. This was conclusively demonstrated using a Closed Loop feedback procedure in which the ensemble code for information presented in the Sample phase of the task was assessed and input to a paradigm that either shortened or extended the temporal delay between Sample and Nonmatch phases of the task as a function of the “strength” or efficacy of the Sample (ensemble) code. The Closed Loop paradigm facilitated task performance in two separate ways: (1) by decreasing the number of weak less distinct, codes that were “at-risk” for errors on long delay (>10 s) trials and (2) extending the capacity to perform correctly on longer delay trials when strong ensemble codes for Sample information were present on the same trial. In addition, two models – linear and nonlinear – for assessing ensemble codes were tested in the Closed Loop paradigm with the nonlinear model showing greater efficiency. The successful application of the Closed Loop feedback in this context makes it apparent that differential hippocampal ensemble coding is a key factor underlying short-term memory, while errors, when they occur, result from neural codes of insufficient representational efficacy to be retained over long delay intervals, thereby causing lack of retrieval.

An erratum to this chapter can be found at http://dx.doi.org/10.1007/978-1-60327-202-5_12

An erratum to this chapter can be found athttp://dx.doi.org/10.1007/978-1-60327-202-5_12

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References

  1. Gerstein GL, Perkel DH (1969) Simultan‑eously recorded trains of action potentials: analysis and functional interpretation. Science 164:828–830.

    Article  CAS  PubMed  Google Scholar 

  2. Abeles M, Gerstein GL (1988) Detecting spatiotemporal firing patterns among simultaneously recorded single neurons. J Neurosci 60:909–924.

    CAS  Google Scholar 

  3. Gochin PM, Colombo M, Dorfman GA, Gerstein GL, Gross CG (1994) Neural ensemble coding in inferior temporal cortex. J Neurophysiol 71:2325–2337.

    Article  CAS  PubMed  Google Scholar 

  4. Georgopoulos AP, Schwartz AB, Kettner RE (1986) Neuronal population encoding of movement direction. Science 233:1416–1419.

    Article  CAS  PubMed  Google Scholar 

  5. Lee D, Port NP, Kruse W, Georgopoulos AP (1998) Neuronal population coding: multielectrode recording in primate cerebral cortex. In: Neuronal ensembles: strategies for recording and decoding. Eichenbaum H, Davis J (Eds), Wiley, New York.

    Google Scholar 

  6. Georgopoulos AP (2000) Neural aspects of cognitive motor control. Curr Opin Neurobiol 10:238–241.

    Article  CAS  PubMed  Google Scholar 

  7. Moran DW, Schwartz AB (1999) Motor cortical activity during drawing movements: ­population representation during spiral ­tracing. J Neurophysiol 82:2693–2704.

    Article  CAS  PubMed  Google Scholar 

  8. Schwartz AB, Moran DW (1999) Motor cortical activity during drawing movements: population representation during lemniscate tracing. J Neurophysiol 82:2705–2718.

    Article  CAS  PubMed  Google Scholar 

  9. van Hemmen JL, Schwartz AB (2008) Population vector code: a geometric universal as actuator. Biol Cybern 98:509–518.

    Article  PubMed  Google Scholar 

  10. Donoghue JP, Nurmikko A, Friehs G, Black M (2004) Development of neuromotor prostheses for humans. Suppl Clin Neurophysiol 57:592–606.

    Article  PubMed  Google Scholar 

  11. Friehs GM, Zerris VA, Ojakangas CL, Fellows MR, Donoghue JP (2004) Brain-machine and brain-computer interfaces. Stroke 35:2702–2705.

    Article  PubMed  Google Scholar 

  12. Chapin JK, Moxon KA, Markowitz RS, Nicolelis MA (1999) Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex. Nature Neurosci 2:664–670.

    Article  CAS  PubMed  Google Scholar 

  13. Wessberg J, Nicolelis MA (2004) Optimizing a linear algorithm for real-time robotic ­control using chronic cortical ensemble recordings in monkeys. J Cogn Neurosci 16:1022–1035.

    Article  PubMed  Google Scholar 

  14. Velliste M, Perel S, Spalding MC, Whitford AS, Schwartz AB (2008) Cortical control of a prosthetic arm for self-feeding. Nature 453:1098–1101.

    Article  CAS  PubMed  Google Scholar 

  15. Schwartz AB, Cui XT, Weber DJ, Moran DW (2006) Brain-controlled interfaces: movement restoration with neural prosthetics. Neuron 52:205–220.

    Article  CAS  PubMed  Google Scholar 

  16. Talwar SK, Xu S, Hawley ES, Weiss SA, Moxon KA, Chapin JK (2002) Rat navigation guided by remote control. Nature 417:37–38.

    Article  CAS  PubMed  Google Scholar 

  17. Ergorul C, Eichenbaum H (2004) The hippocampus and memory for “what,” “where,” and “when”. Learn Mem 11:397–405.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Stepniewska I, Fang PC, Kaas JH (2005) Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos. Proc Natl Acad Sci USA 102:4878–4883.

    Article  CAS  PubMed  Google Scholar 

  19. Freedman DJ, Riesenhuber M, Poggio T, Miller EK (2002) Visual categorization and the primate prefrontal cortex: neurophysiology and behavior. J Neurophysiol 88:929–941.

    Article  PubMed  Google Scholar 

  20. Wallis JD, Miller EK (2003) Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci 18:2069–2081.

    Article  PubMed  Google Scholar 

  21. Eldawlatly S, Jin R, Oweiss KG (2008) Identifying functional connectivity in large-scale neural ensemble recordings: a multiscale data mining approach. Neural Comput 21:450–477.

    Article  Google Scholar 

  22. Wilson IA, Ikonen S, Gurevicius K, McMahan RW, Gallagher M, Eichenbaum H, Tanila H (2005) Place cells of aged rats in two visually identical compartments. Neurobiol Aging 26:1099–1106.

    Article  CAS  PubMed  Google Scholar 

  23. Bilkey DK, Clearwater JM (2005) The dynamic nature of spatial encoding in the hippocampus. Behav Neurosci 119:1533–1545.

    Article  PubMed  Google Scholar 

  24. Touretzky DS, Weisman WE, Fuhs MC, Skaggs WE, Fenton AA, Muller RU (2005) Deforming the hippocampal map. Hippocampus 15:41–55.

    Article  PubMed  Google Scholar 

  25. Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145–156.

    Article  CAS  PubMed  Google Scholar 

  26. Ribeiro S, Nicolelis MA (2004) Reverberation, storage, and postsynaptic propagation of memories during sleep. Learn Mem 11:686–696.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309:619–623.

    Article  CAS  PubMed  Google Scholar 

  28. Buzsaki G (2005) Theta rhythm of navigation: link between path integration and ­landmark navigation, episodic and semantic memory. Hippocampus 15:827–840.

    Article  PubMed  Google Scholar 

  29. Battaglia FP, Sutherland GR, McNaughton BL (2004) Local sensory cues and place cell directionality: additional evidence of prospective coding in the hippocampus. J Neurosci 24:4541–4550.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Huxter J, Burgess N, O’Keefe J (2003) Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425:828–832.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Knierim JJ, Rao G (2003) Distal landmarks and hippocampal place cells: effects of relative translation versus rotation. Hippocampus 13:604–617.

    Article  PubMed  Google Scholar 

  32. de Hoz L, Martin SJ, Morris RG (2004) Forgetting, reminding, and remembering: the retrieval of lost spatial memory. PLoS Biol 2:E225.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Donchin E (1966) A multivariate approach to the analysis of average evoked potentials. IEEE Trans Bio-Med Eng 19:457–463.

    Google Scholar 

  34. Hampson RE, Simeral JD, Deadwyler SA (2001) What ensemble recordings reveal about functional hippocampal cell encoding. Prog Brain Res 130:345–357.

    Article  CAS  PubMed  Google Scholar 

  35. Barbieri R, Frank LM, Nguyen DP, Quirk MC, Solo V, Wilson MA, Brown EN (2004) Dynamic analyses of information encoding in neural ensembles. Neural Comput 16:277–307.

    Article  PubMed  Google Scholar 

  36. Truccolo W, Eden UT, Fellows MR, Donoghue JP, Brown EN (2005) A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. J Neurophysiol 93:1074–1089.

    Article  PubMed  Google Scholar 

  37. Lebedev MA, O’Doherty JE, Nicolelis MA (2008) Decoding of temporal intervals from cortical ensemble activity. J Neurophysiol 99:166–186.

    Article  PubMed  Google Scholar 

  38. Bonifazi P, Ruaro ME, Torre V (2005) Statistical properties of information processing in neuronal networks. Eur J Neurosci 22:2953–2964.

    Article  PubMed  Google Scholar 

  39. Brown SL, Joseph J, Stopfer M (2005) Encoding a temporally structured stimulus with a temporally structured neural representation. Nat Neurosci 8:1568–1576.

    Article  CAS  PubMed  Google Scholar 

  40. Deadwyler SA, Bunn T, Hampson RE (1996) Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats. J Neurosci 16:354–372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hampson RE, Simeral JD, Deadwyler SA (1999) Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402:610–614.

    Article  CAS  PubMed  Google Scholar 

  42. Hampson RE, Simeral JD, Deadwyler SA (2005) Cognitive processes in replacement brain parts: a code for all reasons. In: Toward replacement parts for the brain: implantable biomimetic electronics as neural prosthesis. Berger TW, Glanzman DL (Eds), MIT Press, Cambridge, MA, pp 111–128.

    Google Scholar 

  43. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27:623–633.

    Article  CAS  PubMed  Google Scholar 

  44. Deadwyler SA, Hampson RE (2004) Differential but complementary mnemonic functions of the hippocampus and subiculum. Neuron 42:465–476.

    Article  CAS  PubMed  Google Scholar 

  45. Hampson RE, Simeral JD, Deadwyler SA (2008) Neural population recording in behaving animals: constituents of the neural code for behavior. In: Neural population encoding Holscher C, Munk MH (Eds), Cambridge University Press, Cambridge, UK.

    Google Scholar 

  46. Hampson RE, Deadwyler SA (1996) Ensemble codes involving hippocampal neurons are at risk during delayed performance tests. Proc Natl Acad Sci USA 93:13487–13493.

    Article  CAS  PubMed  Google Scholar 

  47. Simeral JD, Hampson RE, Deadwyler SA (2006) Behaviorally relevant neural codes in hippocampal ensembles: detection on single trials. In: Synaptic plasticity: from basic mechanisms to clinical applications. Baudry M, Bi X, Schreiber S (Eds), MIT Press, Camridge, MA.

    Google Scholar 

  48. Berger TW, Ahuja A, Courellis SH, Deadwyler SA, Erinjippurath G, Gerhardt GA, Gholmieh G, Granacki JJ, Hampson R, Hsaio MC, LaCoss J, Marmarelis VZ, Nasiatka P, Srinivasan V, Song D, Tanguay AR, Wills J (2005) Restoring lost cognitive function. IEEE Eng Med Biol Mag 24:30–44.

    Article  PubMed  Google Scholar 

  49. Stevens J (2002) Applied multivariate statistics for the social sciences. Lawrence Erlbaum Associates, Hillsdale.

    Google Scholar 

  50. Rao CR (2002) Linear statistical inference and its applications. Wiley, New York.

    Google Scholar 

  51. Deadwyler SA, Goonawardena AV, Hampson RE (2007) Short-term memory is modulated by the spontaneous release of endocannabinoids: evidence from hippocampal population codes. Behav Pharmacol 18:571–580.

    Article  CAS  PubMed  Google Scholar 

  52. Deadwyler SA, Hampson RE (2008) Endocannabinoids modulate encoding of sequential memory in the rat hippocampus. Psychopharmacology (Berl) 198:577–586.

    Article  CAS  Google Scholar 

  53. Song D, Chan RM, Marmarelis VZ, Hampson RE, Deadwyler SA, Berger TW (2006) Physiologically plausible stochastic nonlinear kernel models of spike train to spike train transformation. Conf Proc IEEE Eng Med Biol Soc 1:6129–6132.

    Article  Google Scholar 

  54. Zanos TP, Courellis SH, Hampson RE, Deadwyler SA, Marmarelis VZ, Berger TW (2006) A multi-input modeling approach to quantify hippocampal nonlinear dynamic transformations. Conf Proc IEEE Eng Med Biol Soc 1:4967–4970.

    Article  Google Scholar 

  55. Song D, Chan RH, Marmarelis VZ, Hampson RE, Deadwyler SA, Berger TW (2007) Nonlinear dynamic modeling of spike train transformations for hippocampal-cortical prostheses. IEEE Trans Biomed Eng 54:1053–1066.

    Article  PubMed  Google Scholar 

  56. Zanos TP, Courellis SH, Berger TW, Hampson RE, Deadwyler SA, Marmarelis VZ (2008) Nonlinear modeling of causal interrelationships in neuronal ensembles. IEEE Trans Neural Syst Rehabil Eng 16:336–352.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Marmarelis VZ, Berger TW (2005) General methodology for nonlinear modeling of neural systems with Poisson point-process inputs. Math Biosci 196:1–13.

    Article  CAS  PubMed  Google Scholar 

  58. Andersen P, Soleng AF, Raastad M (2000) The hippocampal lamella hypothesis revisited. Brain Res 886:165–171.

    Article  CAS  PubMed  Google Scholar 

  59. Laubach M, Wessberg J, Nicolelis MA (2000) Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405:567–571.

    Article  CAS  PubMed  Google Scholar 

  60. Hampson RE, Deadwyler SA (1999) Pitfalls and problems in the analysis of neuronal ensemble recordings during performance of a behavioral task. In: Methods for simultaneous neuronal ensemble recordings, Nicolelis M (Ed), Academic Press, New York, pp 229–248.

    Google Scholar 

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Acknowledgments

The authors thank the following for assistance with the project: David B. King, Vernell Collins, Rodrigo A. España, and Lihong Shi. This work was supported by NIH grants MH613972 and DA08549 to R.E.H., NSF BMES-ERC and NIH/NIBIB-BMSR to T.W.B. and DA07625 and DARPA contract (SPAWAR) N66001-09-C-2080 to S.A.D.

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Correspondence to Sam A. Deadwyler .

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Hampson, R.E. et al. (2011). Cognitively Relevant Recoding in Hippocampus: Beneficial Feedback of Ensemble Codes in a Closed Loop Paradigm. In: Vertes, R., Stackman Jr., R. (eds) Electrophysiological Recording Techniques. Neuromethods, vol 54. Humana, Totowa, NJ. https://doi.org/10.1007/978-1-60327-202-5_9

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  • DOI: https://doi.org/10.1007/978-1-60327-202-5_9

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  • Publisher Name: Humana, Totowa, NJ

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