Effects of Ketamine on Basal Gamma Band Oscillation and Sensory Gating in Prefrontal Cortex of Awake Rats
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摘要
Gamma band oscillation(GBO) and sensory gating(SG) are associated with many cognitive functions.Ketamine induces deficits of GBO and SG in the prefrontal cortex(PFC). However, the time-courses of the effects of different doses of ketamine on GBO power and SG are poorly understood. Studies have indicated that GBO power and SG have a common substrate for their generation and abnormalities. In this study, we found that(1) ketamine administration increased GBO power in the PFC in rats differently in the low-and high-dose groups;(2) auditory SG was significantly lower than baseline in the 30 mg/kg and 60 mg/kg groups, but not in the 15 mg/kg and 120 mg/kg groups; and(3) changes in SG and basal GBO power were significantly correlated in awake rats. These results indicate a relationship between mechanisms underlying auditory SG and GBO power.
Gamma band oscillation(GBO) and sensory gating(SG) are associated with many cognitive functions.Ketamine induces deficits of GBO and SG in the prefrontal cortex(PFC). However, the time-courses of the effects of different doses of ketamine on GBO power and SG are poorly understood. Studies have indicated that GBO power and SG have a common substrate for their generation and abnormalities. In this study, we found that(1) ketamine administration increased GBO power in the PFC in rats differently in the low-and high-dose groups;(2) auditory SG was significantly lower than baseline in the 30 mg/kg and 60 mg/kg groups, but not in the 15 mg/kg and 120 mg/kg groups; and(3) changes in SG and basal GBO power were significantly correlated in awake rats. These results indicate a relationship between mechanisms underlying auditory SG and GBO power.
Gamma band oscillation(GBO) and sensory gating(SG) are associated with many cognitive functions.Ketamine induces deficits of GBO and SG in the prefrontal cortex(PFC). However, the time-courses of the effects of different doses of ketamine on GBO power and SG are poorly understood. Studies have indicated that GBO power and SG have a common substrate for their generation and abnormalities. In this study, we found that(1) ketamine administration increased GBO power in the PFC in rats differently in the low-and high-dose groups;(2) auditory SG was significantly lower than baseline in the 30 mg/kg and 60 mg/kg groups, but not in the 15 mg/kg and 120 mg/kg groups; and(3) changes in SG and basal GBO power were significantly correlated in awake rats. These results indicate a relationship between mechanisms underlying auditory SG and GBO power.
引文
1.Hughes JR.Gamma,fast,and ultrafast waves of the brain:their relationships with epilepsy and behavior.Epilepsy Behav 2008,13:25-31.
2.Tallon-Baudry C,Bertrand O,Peronnet F,Pernier J.Induced gamma-band activity during the delay of a visual short-term memory task in humans.J Neurosci 1998,18:4244-4254.
3.Haenschel C,Bittner RA,Waltz J,Haertling F,Wibral M,Singer W,et al.Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia.J Neurosci 2009,29:9481-9489.
4.Trinkle-Mulcahy L,Andrews PD,Wickramasinghe S,Sleeman J,Prescott A,Lam YW,et al.Time-lapse imaging reveals dynamic relocalization of PP1 gamma throughout the mammalian cell cycle.Mol Biol Cell 2003,14:107-117.
5.Cho RY,Konecky RO,Carter CS.Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia.Proc Natl Acad Sci U S A 2006,103:19878-19883.
6.Li B,Cui LB,Xi YB,Friston KJ,Guo F,Wang HN,et al.Abnormal effective connectivity in the brain is involved in auditory verbal hallucinations in schizophrenia.Neurosci Bull2017,33:281-291.
7.Gandal MJ,Edgar JC,Klook K,Siegel SJ.Gamma synchrony:towards a translational biomarker for the treatment-resistant symptoms of schizophrenia.Neuropharmacology 2012,62:1504-1518.
8.Adler LE,Pachtman E,Franks RD,Pecevich M,Waldo MC,Freedman R.Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia.Biol Psychiatry 1982,17:639-654.
9.Dissanayake DW,Mason R,Marsden CA.Sensory gating,cannabinoids and schizophrenia.Neuropharmacology 2013,67:66-77.
10.Adler LE,Olincy A,Waldo M,Harris JG,Griffith J,Stevens K,et al.Schizophrenia,sensory gating,and nicotinic receptors.Schizophr Bull 1998,24:189-202.
11.Cullum CM,Harris JG,Waldo MC,Smernoff E,Madison A,Nagamoto HT,et al.Neurophysiological and neuropsychological evidence for attentional dysfunction in schizophrenia.Schizophr Res 1993,10:131-141.
12.Bobo WV,Voort JL,Croarkin PE,Leung JG,Tye SJ,Frye MA.Ketamine for treatment-resistant unipolar and bipolar major depression:critical review and implications for clinical practice.Depress Anxiety 2016,33:698-710.
13.Mathew SJ,Shah A,Lapidus K,Clark C,Jarun N,Ostermeyer B,et al.Ketamine for treatment-resistant unipolar depression:current evidence.CNS Drugs 2012,26:189-204.
14.Carlson PJ,Diazgranados N,Nugent AC,Ibrahim L,Luckenbaugh DA,Brutsche N,et al.Neural correlates of rapid antidepressant response to ketamine in treatment-resistant unipolar depression:a preliminary positron emission tomography study.Biol Psychiatry 2013,73:1213-1221.
15.Frohlich J,Van Horn JD.Reviewing the ketamine model for schizophrenia.J Psychopharmacol 2014,28:287-302.
16.Mion G,Villevieille T.Ketamine pharmacology:an update(pharmacodynamics and molecular aspects,recent findings).CNSNeurosci Ther 2013,19:370-380.
17.Morgan CJ,Curran HV,Independent Scientific Committee on D.Ketamine use:a review.Addiction 2012,107:27-38.
18.Johansson C,Jackson DM,Svensson L.The atypical antipsychotic,remoxipride,blocks phencyclidine-induced disruption of prepulse inhibition in the rat.Psychopharmacology(Berl)1994,116:437-442.
19.Wiley JL.Clozapine’s effects on phencyclidine-induced disruption of prepulse inhibition of the acoustic startle response.Pharmacol Biochem Behav 1994,49:1025-1028.
20.Reijmers LG,Vanderheyden PM,Peeters BW.Changes in prepulse inhibition after local administration of NMDA receptor ligands in the core region of the rat nucleus accumbens.Eur JPharmacol 1995,272:131-138.
21.Hiyoshi T,Kambe D,Karasawa J,Chaki S.Differential effects of NMDA receptor antagonists at lower and higher doses on basal gamma band oscillation power in rat cortical electroencephalograms.Neuropharmacology 2014,85:384-396.
22.Hakami T,Jones NC,Tolmacheva EA,Gaudias J,Chaumont J,Salzberg M,et al.NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness.PLo SOne 2009,4:e6755.
23.Sachidhanandam S,Sermet BS,Petersen CC.Parvalbuminexpressing GABAergic neurons in mouse barrel cortex contribute to gating a goal-directed sensorimotor transformation.Cell Rep2016.
24.Gonzalez-Burgos G,Lewis DA.NMDA receptor hypofunction,parvalbumin-positive neurons,and cortical gamma oscillations in schizophrenia.Schizophr Bull 2012,38:950-957.
25.Gonzalez-Burgos G,Lewis DA.GABA neurons and the mechanisms of network oscillations:implications for understanding cortical dysfunction in schizophrenia.Schizophr Bull 2008,34:944-961.
26.Carlen M,Meletis K,Siegle JH,Cardin JA,Futai K,VierlingClaassen D,et al.A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior.Mol Psychiatry 2012,17:537-548.
27.Homayoun H,Moghaddam B.NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons.J Neurosci 2007,27:11496-11500.
28.Miller CL,Freedman R.Medial septal neuron activity in relation to an auditory sensory gating paradigm.Neuroscience 1993,55:373-380.
29.Miller CL,Freedman R.The activity of hippocampal interneurons and pyramidal cells during the response of the hippocampus to repeated auditory stimuli.Neuroscience 1995,69:371-381.
30.Moxon KA,Gerhardt GA,Adler LE.Dopaminergic modulation of the P50 auditory-evoked potential in a computer model of the CA3 region of the hippocampus:its relationship to sensory gating in schizophrenia.Biol Cybern 2003,88:265-275.
31.Boutros NN,Belger A.Midlatency evoked potentials attenuation and augmentation reflect different aspects of sensory gating.Biol Psychiatry 1999,45:917-922.
32.Vogels TP,Abbott LF.Gating multiple signals through detailed balance of excitation and inhibition in spiking networks.Nat Neurosci 2009,12:483-491.
33.Inan M,Zhao M,Manuszak M,Karakaya C,Rajadhyaksha AM,Pickel VM,et al.Energy deficit in parvalbumin neurons leads to circuit dysfunction,impaired sensory gating and social disability.Neurobiol Dis 2016,93:35-46.
34.Qi R,Li M,Ma Y,Chen N.State-dependent changes in auditory sensory gating in different cortical areas in rats.PLo S One 2015,10:e0126684.
35.Steriade MM,Mc Carley RW.Brain Control of Wakefulness and Sleep.Springer,2007.
36.Hiyoshi T,Kambe D,Karasawa J,Chaki S.Involvement of glutamatergic and GABAergic transmission in MK-801-increased gamma band oscillation power in rat cortical electroencephalograms.Neuroscience 2014,280:262-274.
37.Kulikova SP,Tolmacheva EA,Anderson P,Gaudias J,Adams BE,Zheng T,et al.Opposite effects of ketamine and deep brain stimulation on rat thalamocortical information processing.Eur JNeurosci 2012,36:3407-3419.
38.Haas DA,Harper DG.Ketamine:a review of its pharmacologic properties and use in ambulatory anesthesia.Anesth Prog 1992,39:61-68.
39.Aroni F,Iacovidou N,Dontas I,Pourzitaki C,Xanthos T.Pharmacological aspects and potential new clinical applications of ketamine:reevaluation of an old drug.J Clin Pharmacol 2009,49:957-964.
40.Giroux MC,Santamaria R,Helie P,Burns P,Beaudry F,Vachon P.Physiological,pharmacokinetic and liver metabolism comparisons between 3-,6-,12-and 18-month-old male Sprague Dawley rats under ketamine-xylazine anesthesia.Exp Anim 2016,65:63-75.
41.Wang XJ.Neurophysiological and computational principles of cortical rhythms in cognition.Physiol Rev 2010,90:1195-1268.
42.Whittington MA,Traub RD,Kopell N,Ermentrout B,Buhl EH.Inhibition-based rhythms:experimental and mathematical observations on network dynamics.Int J Psychophysiol 2000,38:315-336.
43.Mansbach RS,Geyer MA.Parametric determinants in prestimulus modification of acoustic startle:interaction with ketamine.Psychopharmacology(Berl)1991,105:162-168.
44.Dissanayake DW,Zachariou M,Marsden CA,Mason R.Auditory gating in rat hippocampus and medial prefrontal cortex:effect of the cannabinoid agonist WIN55,212-2.Neuropharmacology 2008,55:1397-1404.
45.Jackson ME,Homayoun H,Moghaddam B.NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex.Proc Natl Acad Sci U S A 2004,101:8467-8472.
46.Hu ML,Zong XF,Mann JJ,Zheng JJ,Liao YH,Li ZC,et al.AReview of the Functional and Anatomical Default Mode Network in Schizophrenia.Neurosci Bull 2017,33:73-84.
2.Tallon-Baudry C,Bertrand O,Peronnet F,Pernier J.Induced gamma-band activity during the delay of a visual short-term memory task in humans.J Neurosci 1998,18:4244-4254.
3.Haenschel C,Bittner RA,Waltz J,Haertling F,Wibral M,Singer W,et al.Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia.J Neurosci 2009,29:9481-9489.
4.Trinkle-Mulcahy L,Andrews PD,Wickramasinghe S,Sleeman J,Prescott A,Lam YW,et al.Time-lapse imaging reveals dynamic relocalization of PP1 gamma throughout the mammalian cell cycle.Mol Biol Cell 2003,14:107-117.
5.Cho RY,Konecky RO,Carter CS.Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia.Proc Natl Acad Sci U S A 2006,103:19878-19883.
6.Li B,Cui LB,Xi YB,Friston KJ,Guo F,Wang HN,et al.Abnormal effective connectivity in the brain is involved in auditory verbal hallucinations in schizophrenia.Neurosci Bull2017,33:281-291.
7.Gandal MJ,Edgar JC,Klook K,Siegel SJ.Gamma synchrony:towards a translational biomarker for the treatment-resistant symptoms of schizophrenia.Neuropharmacology 2012,62:1504-1518.
8.Adler LE,Pachtman E,Franks RD,Pecevich M,Waldo MC,Freedman R.Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia.Biol Psychiatry 1982,17:639-654.
9.Dissanayake DW,Mason R,Marsden CA.Sensory gating,cannabinoids and schizophrenia.Neuropharmacology 2013,67:66-77.
10.Adler LE,Olincy A,Waldo M,Harris JG,Griffith J,Stevens K,et al.Schizophrenia,sensory gating,and nicotinic receptors.Schizophr Bull 1998,24:189-202.
11.Cullum CM,Harris JG,Waldo MC,Smernoff E,Madison A,Nagamoto HT,et al.Neurophysiological and neuropsychological evidence for attentional dysfunction in schizophrenia.Schizophr Res 1993,10:131-141.
12.Bobo WV,Voort JL,Croarkin PE,Leung JG,Tye SJ,Frye MA.Ketamine for treatment-resistant unipolar and bipolar major depression:critical review and implications for clinical practice.Depress Anxiety 2016,33:698-710.
13.Mathew SJ,Shah A,Lapidus K,Clark C,Jarun N,Ostermeyer B,et al.Ketamine for treatment-resistant unipolar depression:current evidence.CNS Drugs 2012,26:189-204.
14.Carlson PJ,Diazgranados N,Nugent AC,Ibrahim L,Luckenbaugh DA,Brutsche N,et al.Neural correlates of rapid antidepressant response to ketamine in treatment-resistant unipolar depression:a preliminary positron emission tomography study.Biol Psychiatry 2013,73:1213-1221.
15.Frohlich J,Van Horn JD.Reviewing the ketamine model for schizophrenia.J Psychopharmacol 2014,28:287-302.
16.Mion G,Villevieille T.Ketamine pharmacology:an update(pharmacodynamics and molecular aspects,recent findings).CNSNeurosci Ther 2013,19:370-380.
17.Morgan CJ,Curran HV,Independent Scientific Committee on D.Ketamine use:a review.Addiction 2012,107:27-38.
18.Johansson C,Jackson DM,Svensson L.The atypical antipsychotic,remoxipride,blocks phencyclidine-induced disruption of prepulse inhibition in the rat.Psychopharmacology(Berl)1994,116:437-442.
19.Wiley JL.Clozapine’s effects on phencyclidine-induced disruption of prepulse inhibition of the acoustic startle response.Pharmacol Biochem Behav 1994,49:1025-1028.
20.Reijmers LG,Vanderheyden PM,Peeters BW.Changes in prepulse inhibition after local administration of NMDA receptor ligands in the core region of the rat nucleus accumbens.Eur JPharmacol 1995,272:131-138.
21.Hiyoshi T,Kambe D,Karasawa J,Chaki S.Differential effects of NMDA receptor antagonists at lower and higher doses on basal gamma band oscillation power in rat cortical electroencephalograms.Neuropharmacology 2014,85:384-396.
22.Hakami T,Jones NC,Tolmacheva EA,Gaudias J,Chaumont J,Salzberg M,et al.NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness.PLo SOne 2009,4:e6755.
23.Sachidhanandam S,Sermet BS,Petersen CC.Parvalbuminexpressing GABAergic neurons in mouse barrel cortex contribute to gating a goal-directed sensorimotor transformation.Cell Rep2016.
24.Gonzalez-Burgos G,Lewis DA.NMDA receptor hypofunction,parvalbumin-positive neurons,and cortical gamma oscillations in schizophrenia.Schizophr Bull 2012,38:950-957.
25.Gonzalez-Burgos G,Lewis DA.GABA neurons and the mechanisms of network oscillations:implications for understanding cortical dysfunction in schizophrenia.Schizophr Bull 2008,34:944-961.
26.Carlen M,Meletis K,Siegle JH,Cardin JA,Futai K,VierlingClaassen D,et al.A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior.Mol Psychiatry 2012,17:537-548.
27.Homayoun H,Moghaddam B.NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons.J Neurosci 2007,27:11496-11500.
28.Miller CL,Freedman R.Medial septal neuron activity in relation to an auditory sensory gating paradigm.Neuroscience 1993,55:373-380.
29.Miller CL,Freedman R.The activity of hippocampal interneurons and pyramidal cells during the response of the hippocampus to repeated auditory stimuli.Neuroscience 1995,69:371-381.
30.Moxon KA,Gerhardt GA,Adler LE.Dopaminergic modulation of the P50 auditory-evoked potential in a computer model of the CA3 region of the hippocampus:its relationship to sensory gating in schizophrenia.Biol Cybern 2003,88:265-275.
31.Boutros NN,Belger A.Midlatency evoked potentials attenuation and augmentation reflect different aspects of sensory gating.Biol Psychiatry 1999,45:917-922.
32.Vogels TP,Abbott LF.Gating multiple signals through detailed balance of excitation and inhibition in spiking networks.Nat Neurosci 2009,12:483-491.
33.Inan M,Zhao M,Manuszak M,Karakaya C,Rajadhyaksha AM,Pickel VM,et al.Energy deficit in parvalbumin neurons leads to circuit dysfunction,impaired sensory gating and social disability.Neurobiol Dis 2016,93:35-46.
34.Qi R,Li M,Ma Y,Chen N.State-dependent changes in auditory sensory gating in different cortical areas in rats.PLo S One 2015,10:e0126684.
35.Steriade MM,Mc Carley RW.Brain Control of Wakefulness and Sleep.Springer,2007.
36.Hiyoshi T,Kambe D,Karasawa J,Chaki S.Involvement of glutamatergic and GABAergic transmission in MK-801-increased gamma band oscillation power in rat cortical electroencephalograms.Neuroscience 2014,280:262-274.
37.Kulikova SP,Tolmacheva EA,Anderson P,Gaudias J,Adams BE,Zheng T,et al.Opposite effects of ketamine and deep brain stimulation on rat thalamocortical information processing.Eur JNeurosci 2012,36:3407-3419.
38.Haas DA,Harper DG.Ketamine:a review of its pharmacologic properties and use in ambulatory anesthesia.Anesth Prog 1992,39:61-68.
39.Aroni F,Iacovidou N,Dontas I,Pourzitaki C,Xanthos T.Pharmacological aspects and potential new clinical applications of ketamine:reevaluation of an old drug.J Clin Pharmacol 2009,49:957-964.
40.Giroux MC,Santamaria R,Helie P,Burns P,Beaudry F,Vachon P.Physiological,pharmacokinetic and liver metabolism comparisons between 3-,6-,12-and 18-month-old male Sprague Dawley rats under ketamine-xylazine anesthesia.Exp Anim 2016,65:63-75.
41.Wang XJ.Neurophysiological and computational principles of cortical rhythms in cognition.Physiol Rev 2010,90:1195-1268.
42.Whittington MA,Traub RD,Kopell N,Ermentrout B,Buhl EH.Inhibition-based rhythms:experimental and mathematical observations on network dynamics.Int J Psychophysiol 2000,38:315-336.
43.Mansbach RS,Geyer MA.Parametric determinants in prestimulus modification of acoustic startle:interaction with ketamine.Psychopharmacology(Berl)1991,105:162-168.
44.Dissanayake DW,Zachariou M,Marsden CA,Mason R.Auditory gating in rat hippocampus and medial prefrontal cortex:effect of the cannabinoid agonist WIN55,212-2.Neuropharmacology 2008,55:1397-1404.
45.Jackson ME,Homayoun H,Moghaddam B.NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex.Proc Natl Acad Sci U S A 2004,101:8467-8472.
46.Hu ML,Zong XF,Mann JJ,Zheng JJ,Liao YH,Li ZC,et al.AReview of the Functional and Anatomical Default Mode Network in Schizophrenia.Neurosci Bull 2017,33:73-84.