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01-07-2014 | Original Article

Visual training paired with electrical stimulation of the basal forebrain improves orientation-selective visual acuity in the rat

Authors: Jun Il Kang, Marianne Groleau, Florence Dotigny, Hugo Giguère, Elvire Vaucher

Published in: Brain Structure and Function | Issue 4/2014

Abstract

The cholinergic afferents from the basal forebrain to the primary visual cortex play a key role in visual attention and cortical plasticity. These afferent fibers modulate acute and long-term responses of visual neurons to specific stimuli. The present study evaluates whether this cholinergic modulation of visual neurons results in cortical activity and visual perception changes. Awake adult rats were exposed repeatedly for 2 weeks to an orientation-specific grating with or without coupling this visual stimulation to an electrical stimulation of the basal forebrain. The visual acuity, as measured using a visual water maze before and after the exposure to the orientation-specific grating, was increased in the group of trained rats with simultaneous basal forebrain/visual stimulation. The increase in visual acuity was not observed when visual training or basal forebrain stimulation was performed separately or when cholinergic fibers were selectively lesioned prior to the visual stimulation. The visual evoked potentials show a long-lasting increase in cortical reactivity of the primary visual cortex after coupled visual/cholinergic stimulation, as well as c-Fos immunoreactivity of both pyramidal and GABAergic interneuron. These findings demonstrate that when coupled with visual training, the cholinergic system improves visual performance for the trained orientation probably through enhancement of attentional processes and cortical plasticity in V1 related to the ratio of excitatory/inhibitory inputs. This study opens the possibility of establishing efficient rehabilitation strategies for facilitating visual capacity.

Ahissar M, Hochstein S (1993) Attentional control of early perceptual learning. Proc Natl Acad Sci USA 90(12):5718–5722PubMedCentralPubMedCrossRef

Amar M, Lucas-Meunier E, Baux G, Fossier P (2010) Blockade of different muscarinic receptor subtypes changes the equilibrium between excitation and inhibition in rat visual cortex. Neuroscience 169(4):1610–1620. doi:10.1016/j.neuroscience.2010.06.019 PubMedCrossRef

Andersen GJ, Ni R, Bower JD, Watanabe T (2010) Perceptual learning, aging, and improved visual performance in early stages of visual processing. J Vis 10(13):4. doi:10.1167/10.13.4 PubMedCentralPubMedCrossRef

Bao S, Chan VT, Merzenich MM (2001) Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412(6842):79–83. doi:10.1038/3508358635083586 PubMedCrossRef

Bear MF, Singer W (1986) Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320(6058):172–176. doi:10.1038/320172a0 PubMedCrossRef

Bhattacharyya A, Biessmann F, Veit J, Kretz R, Rainer G (2012) Functional and laminar dissociations between muscarinic and nicotinic cholinergic neuromodulation in the tree shrew primary visual cortex. Eur J Neurosci 35(8):1270–1280. doi:10.1111/j.1460-9568.2012.08052.x PubMedCrossRef

Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G (1998) Endogenous ACh enhances striatal NMDA-responses via M1-like muscarinic receptors and PKC activation. Eur J Neurosci 10(9):2887–2895PubMedCrossRef

Callaway E (2004) Feedforward, feedback and inhibitory connections in primate visual cortex. Neural Networks 17(5–6):625–632. doi:10.1016/j.neunet.2004.04.004 PubMedCrossRef

Christophe E, Roebuck A, Staiger JF, Lavery DJ, Charpak S, Audinat E (2002) Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons. J Neurophysiol 88(3):1318–1327PubMed

Conner JM, Culberson A, Packowski C, Chiba AA, Tuszynski MH (2003) Lesions of the Basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 38(5):819–829. doi:10.1016/S0896-6273(03)00288-5 PubMedCrossRef

Cooke SF, Bear MF (2010) Visual experience induces long-term potentiation in the primary visual cortex. J Neurosci 30(48):16304–16313. doi:10.1523/JNEUROSCI.4333-10.2010 PubMedCentralPubMedCrossRef

Cooke SF, Bear MF (2012) Stimulus-selective response plasticity in the visual cortex: an assay for the assessment of pathophysiology and treatment of cognitive impairment associated with psychiatric disorders. Biol Psychiatry 71(6):487–495. doi:10.1016/j.biopsych.2011.09.006 PubMedCrossRef

Deco G, Thiele A (2011) Cholinergic control of cortical network interactions enables feedback-mediated attentional modulation. Eur J Neurosci 34(1):146–157. doi:10.1111/j.1460-9568.2011.07749.x PubMedCrossRef

Disney AA, Aoki C, Hawken MJ (2012) Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition. J Neurophysiol 108(7):1907–1923. doi:10.1152/jn.00188.2012 PubMedCentralPubMedCrossRef

Dotigny F, Ben Amor AY, Burke M, Vaucher E (2008) Neuromodulatory role of acetylcholine in visually-induced cortical activation: behavioral and neuroanatomical correlates. Neuroscience 154(4):1607–1618. doi:10.1016/j.neuroscience.2008.04.030 PubMedCrossRef

Dringenberg HC, Hamze B, Wilson A, Speechley W, Kuo MC (2006) Heterosynaptic facilitation of in vivo thalamocortical long-term potentiation in the adult rat visual cortex by acetylcholine. Cereb Cortex 17(4):839–848. doi:10.1093/cercor/bhk038 PubMedCrossRef

Fahle M (2004) Perceptual learning: a case for early selection. J Vis 4(10):879–890PubMedCrossRef

Fiorentini A, Berardi N (1980) Perceptual learning specific for orientation and spatial frequency. Nature 287(5777):43–44PubMedCrossRef

Frenkel MY, Sawtell NB, Diogo AC, Yoon B, Neve RL, Bear MF (2006) Instructive effect of visual experience in mouse visual cortex. Neuron 51(3):339–349. doi:10.1016/j.neuron.2006.06.026 PubMedCrossRef

Gandhi SP, Yanagawa Y, Stryker MP (2008) Delayed plasticity of inhibitory neurons in developing visual cortex. Proc Natl Acad Sci 105(43):16797–16802. doi:10.1073/pnas.0806159105 PubMedCentralPubMedCrossRef

Gaykema RP, Luiten PG, Nyakas C, Traber J (1990) Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293(1):103–124PubMedCrossRef

Gil Z, Connors BW, Amitai Y (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19(3):679–686PubMedCrossRef

Gilbert CD, Sigman M, Crist RE (2001) The neural basis of perceptual learning. Neuron 31(5):681–697PubMedCrossRef

Girman SV, Sauve Y, Lund RD (1999) Receptive field properties of single neurons in rat primary visual cortex. J Neurophysiol 82(1):301–311PubMed

Goard M, Dan Y (2009) Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12(11):1444–1449. doi:10.1038/nn.2402 PubMedCentralPubMedCrossRef

Gonchar Y, Burkhalter A (2003) Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex. J Neurosci 23(34):10904–10912PubMed

Greuel JM, Luhmann HJ, Singer W (1988) Pharmacological induction of use-dependent receptive field modifications in the visual cortex. Science 242(4875):74–77PubMedCrossRef

Gu Q (2003) Contribution of acetylcholine to visual cortex plasticity. Neurobiol Learn Mem 80(3):291–301. doi:10.1016/s1074-7427(03)00073-x PubMedCrossRef

Herrero JL, Roberts MJ, Delicato LS, Gieselmann MA, Dayan P, Thiele A (2008) Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature 454(7208):1110–1114. pii: nature07141PubMedCentralPubMedCrossRef

Kaczmarek L, Chaudhuri A (1997) Sensory regulation of immediate-early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity. Brain Res Brain Res Rev 23(3):237–256PubMedCrossRef

Kang JI, Vaucher E (2009) Cholinergic pairing with visual activation results in long-term enhancement of visual evoked potentials. PLoS ONE 4(6):e5995. doi:10.1371/journal.pone.0005995 PubMedCentralPubMedCrossRef

Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279(5357):1714–1718. doi:10.1126/science.279.5357.1714 PubMedCrossRef

Kimura F, Fukuda M, Tsumoto T (1999) Acetylcholine suppresses the spread of excitation in the visual cortex revealed by optical recording: possible differential effect depending on the source of input. Eur J Neurosci 11(10):3597–3609PubMedCrossRef

Kocharyan A, Fernandes P, Tong XK, Vaucher E, Hamel E (2008) Specific subtypes of cortical GABA interneurons contribute to the neurovascular coupling response to basal forebrain stimulation. J Cerebral Blood Flow Metab Off J Int Soc Cerebral Blood Flow Metab 28(2):221–231. doi:10.1038/sj.jcbfm.9600558 CrossRef

Kosovicheva AA, Sheremata SL, Rokem A, Landau AN, Silver MA (2012) Cholinergic enhancement reduces orientation-specific surround suppression but not visual crowding. Frontiers Behav Neurosci 6:61. doi:10.3389/fnbeh.2012.00061 CrossRef

Kruglikov I, Rudy B (2008) Perisomatic GABA release and thalamocortical integration onto neocortical excitatory cells are regulated by neuromodulators. Neuron 58(6):911–924 Pii: S0896-6273(08)00378-4PubMedCentralPubMedCrossRef

Kuczewski N, Aztiria E, Gautam D, Wess J, Domenici L (2005) Acetylcholine modulates cortical synaptic transmission via different muscarinic receptors, as studied with receptor knockout mice. J Physiol 566(Pt 3):907–919. doi:10.1113/jphysiol.2005.089987 PubMedCentralPubMedCrossRef

Laplante F, Morin Y, Quirion R, Vaucher E (2005) Acetylcholine release is elicited in the visual cortex, but not in the prefrontal cortex, by patterned visual stimulation: a dual microdialysis study with functional correlates in the rat brain. Neuroscience 132(2):501–510. doi:10.1016/j.neuroscience.2004.11.059 PubMedCrossRef

Li W, Piëch V, Gilbert CD (2004) Perceptual learning and top-down influences in primary visual cortex. Nat Neurosci 7(6):651–657. doi:10.1038/nn1255 PubMedCentralPubMedCrossRef

Lucas-Meunier E, Monier C, Amar M, Baux G, Fregnac Y, Fossier P (2009) Involvement of nicotinic and muscarinic receptors in the endogenous cholinergic modulation of the balance between excitation and inhibition in the young rat visual cortex. Cereb Cortex 19(10):2411–2427. doi:10.1093/cercor/bhn258 PubMedCrossRef

Morishita H, Miwa JM, Heintz N, Hensch TK (2010) Lynx1, a cholinergic brake, limits plasticity in adult visual cortex. Science 330 (6008):1238–1240. doi:10.1126/science.1195320

Newman EL, Gupta K, Climer JR, Monaghan CK, Hasselmo ME (2012) Cholinergic modulation of cognitive processing: insights drawn from computational models. Frontiers Behav Neurosci 6:24. doi:10.3389/fnbeh.2012.00024 CrossRef

Oldford E, Castro-Alamancos MA (2003) Input-specific effects of acetylcholine on sensory and intracortical evoked responses in the “barrel cortex” in vivo. Neuroscience 117(3):769–778PubMedCrossRef

Origlia N, Kuczewski N, Aztiria E, Gautam D, Wess J, Domenici L (2006) Muscarinic acetylcholine receptor knockout mice show distinct synaptic plasticity impairments in the visual cortex. J Physiol 577(Pt 3):829–840. doi:10.1113/jphysiol.2006.117119 PubMedCentralPubMedCrossRef

Paxinos G, Watson CR (1995) The rat brain in stereotaxic coordinates, 3rd edn. Academic Press, Sydney

Prusky GT, West PW, Douglas RM (2000) Behavioral assessment of visual acuity in mice and rats. Vision Res 40(16):2201–2209. doi:10.1016/S0042-6989(00)00081-X PubMedCrossRef

Recanzone GH, Schreiner CE, Merzenich MM (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 13(1):87–103PubMed

Reed A, Riley J, Carraway R, Carrasco A, Perez C, Jakkamsetti V, Kilgard MP (2011) Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 70(1):121–131. doi:10.1016/j.neuron.2011.02.038 PubMedCrossRef

Roberts MJ, Zinke W, Guo K, Robertson R, McDonald JS, Thiele A (2005) Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. J Neurophysiol 93(4):2062–2072. doi:10.1152/jn.00911.2004 PubMedCentralPubMedCrossRef

Roelfsema PR, van Ooyen A, Watanabe T (2010) Perceptual learning rules based on reinforcers and attention. Trends Cogn Sci 14 (2):64–71. doi:10.1016/j.tics.2009.11.005

Rokem A, Silver MA (2010) Cholinergic enhancement augments magnitude and specificity of visual perceptual learning in healthy humans. Current biology CB 20(19):1723–1728. doi:10.1016/j.cub.2010.08.027 PubMedCentralPubMedCrossRef

Runyan CA, Schummers J, Van Wart A, Kuhlman SJ, Wilson NR, Huang ZJ, Sur M (2010) Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron 67(5):847–857. doi:10.1016/j.neuron.2010.08.006 PubMedCentralPubMedCrossRef

Sabel BA, Henrich-Noack P, Fedorov A, Gall C (2011) Vision restoration after brain and retina damage: the “residual vision activation theory”. Prog Brain Res 192:199–262. doi:10.1016/b978-0-444-53355-5.00013-0 PubMedCrossRef

Sale A, De Pasquale R, Bonaccorsi J, Pietra G, Olivieri D, Berardi N, Maffei L (2011) Visual perceptual learning induces long-term potentiation in the visual cortex. Neuroscience 172:219–225. doi:10.1016/j.neuroscience.2010.10.078 PubMedCrossRef

Salgado H, Bellay T, Nichols JA, Bose M, Martinolich L, Perrotti L, Atzori M (2007) Muscarinic M2 and M1 receptors reduce GABA release by Ca²⁺ channel modulation through activation of PI3 K/Ca²⁺ -independent and PLC/Ca²⁺ -dependent PKC. J Neurophysiol 98 (2):952–965. doi:10.1152/jn.00060.2007

Sarter M, Hasselmo ME, Bruno JP, Givens B (2005) Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res Rev 48(1):98–111. doi:10.1016/j.brainresrev.2004.08.006

Sasaki Y, Nanez JE, Watanabe T (2010) Advances in visual perceptual learning and plasticity. Nat Rev Neurosci 11 (1):53–60. doi:10.1038/nrn2737

Schoups A, Vogels R, Qian N, Orban G (2001) Practising orientation identification improves orientation coding in V1 neurons. Nature 412(6846):549–553. doi:10.1038/35087601 PubMedCrossRef

Seitz A, Watanabe T (2005) A unified model for perceptual learning. Trends Cogn Sci 9(7):329–334. doi:10.1016/j.tics.2005.05.010 PubMedCrossRef

Silver MA, Shenhav A, D’Esposito M (2008) Cholinergic enhancement reduces spatial spread of visual responses in human early visual cortex. Neuron 60(5):904–914. doi:10.1016/j.neuron.2008.09.038 PubMedCentralPubMedCrossRef

Soma S, Shimegi S, Osaki H, Sato H (2012) Cholinergic modulation of response gain in the primary visual cortex of the macaque. J Neurophysiol 107(1):283–291. doi:10.1152/jn.00330.2011 PubMedCrossRef

Thiele A, Herrero JL, Distler C, Hoffmann KP (2012) Contribution of cholinergic and GABAergic mechanisms to direction tuning, discriminability, response reliability, and neuronal rate correlations in macaque middle temporal area. J Neurosci 32(47):16602–16615. doi:10.1523/JNEUROSCI.0554-12.2012 PubMedCrossRef

Vaucher E, Borredon J, Bonvento G, Seylaz J, Lacombe P (1997) Autoradiographic evidence for flow-metabolism uncoupling during stimulation of the nucleus basalis of Meynert in the conscious rat. J Cerebral Blood Flow and Metab Off J Int Soc Cerebral Blood Flow Metab 17(6):686–694. doi:10.1097/00004647-199706000-00010 CrossRef

Vidnyanszky Z, Sohn W (2005) Learning to suppress task-irrelevant visual stimuli with attention. Vision Res 45(6):677–685. doi:10.1016/j.visres.2004.10.009 PubMedCrossRef

Yazaki-Sugiyama Y, Kang S, Cateau H, Fukai T, Hensch TK (2009) Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 462(7270):218–221. doi:10.1038/nature08485

Zinke W, Roberts MJ, Guo K, McDonald JS, Robertson R, Thiele A (2006) Cholinergic modulation of response properties and orientation tuning of neurons in primary visual cortex of anaesthetized Marmoset monkeys. Eur J Neurosci 24(1):314–328. doi:10.1111/j.1460-9568.2006.04882.x PubMedCentralPubMedCrossRef

Title: Visual training paired with electrical stimulation of the basal forebrain improves orientation-selective visual acuity in the rat
Authors: Jun Il Kang
Marianne Groleau
Florence Dotigny
Hugo Giguère
Elvire Vaucher
Publication date: 01-07-2014
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2014
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-013-0582-y

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Visual training paired with electrical stimulation of the basal forebrain improves orientation-selective visual acuity in the rat

Abstract

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