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Primed-bursts induced long-term potentiation in rat visual cortex: effects of dark-rearing
Brain Research 851 Ž1999. 148–153 www.elsevier.comrlocaterbres
Research report
Primed-bursts induced long-term potentiation in rat visual cortex: effects of dark-rearing Nafiseh Atapour a
a,b,)
, Hossein Esteky a , Yaghoub Fathollahi c , Farshad Alizadeh Mansouri
a
Department of Physiology, School of Medicine, Shaheed Beheshti UniÕersity of Medical Sciences, Tehran, Iran b Department of Physiology, School of Medicine, Kerman UniÕersity of Medical Sciences, Kerman, Iran c Department of Physiology, School of Medical Sciences, Tarbiat Modarress UniÕersity, Tehran, Iran Accepted 21 September 1999
Abstract Theta burst stimulation ŽTBS. and primed bursts ŽPBs. stimulation are among the effective tetanic stimulations for induction of long-term potentiation ŽLTP. in the hippocampus. Recent studies have indicated that TBS is effective in LTP induction of layer III synapses of neocortex, only if applied to layer IV. However, the possibility of neocortical LTP induction using PBs has not been investigated yet. Sensory deprivation greatly influences the development of neocortex. According to the effect of sensory deprivation on synaptic plasticity of developing neocortex, we studied the induction of LTP by PBs in visual cortical slices of control and dark-reared rats. The results showed that application of PBs to layer IV could effectively induce LTP of layer IIrIII field potentials. These potentials are consisted of two components: pEPSP1 Žpopulation excitatory postsynaptic potential 1. and pEPSP2 . In control slices PBs led to selective potentiation of pEPSP2 . Visual deprivation increased the incidence of LTP of pEPSP1 and decreased the amount of LTP of pEPSP2 . These findings showed that PBs could be used as an effective tetanic stimulation to study the synaptic plasticity in neocortex. The effects of visual deprivation on PBs-induced LTP are consistent with its role in the development of excitatory system in neocortex. q 1999 Published by Elsevier Science B.V. All rights reserved. Keywords: Tetanic stimulation; Brain slice; Plasticity; Field potential; Dark-rearing
1. Introduction The normal development of visual cortex during early postnatal period could be altered by manipulation of visual experience. For example, dark-rearing delays the loss of N-methyl-D-aspartate ŽNMDA. receptor function in kitten w13x and NMDA receptor-mediated currents in rat visual cortex w7x. Also, visual deprivation decreases long-term potentiation ŽLTP. in visual cortical slices of 17- to 21day-old rats w6x and increases it in adult rat neocortex w20x. LTP is a long-lasting increase in synaptic efficacy elicited by brief, high frequency bursts of synaptic activation. Activation of NMDA receptors is essential for the induction of neocortical LTP w4,17x. Different studies on rat neocortex have shown that the activity of NMDA system increases to a maximum during the second and third postnatal weeks and then declines slightly in adulthood w7,14–16,24,26x. Critical period for maximum LTP ) C orresponding author. [email protected]
Fax:
q 98-341-55098;
e-m ail:
induction coincides temporally with a ‘‘developmental window’’ within which activity of NMDA system is enhanced w17,24x. GABAergic system matures gradually during the first postnatal month w23x. During the ‘‘developmental window’’ the GABAergic inhibition is immature w24x. Maturation of GABAergic inhibition decreases the neocortical susceptibility for LTP induction w17x. Slight inhibition of this system has been shown to be essential for the activation of NMDA receptors and neocortical LTP induction w4,5x. The induction of LTP in the neocortex is more difficult than in the hippocampus w31x. Theta burst stimulation ŽTBS. and primed bursts ŽPBs. tetanic stimulation are widely used in the induction of LTP in the hippocampus w9,12,21,25,29x. It has been shown that in the absence of GABA A blockers, TBS can induce LTP in neocortical layer III synapses only if applied to layer IV and not to the white matter w18x. Application of TBS to the white matter could be effective in the neocortex only if GABA A receptors are blocked w18x. According to the Kirkwood and Bear plasticity gate hypothesis, layer IV inhibitory circuits act
0006-8993r99r$ - see front matter q 1999 Published by Elsevier Science B.V. All rights reserved. PII: S 0 0 0 6 - 8 9 9 3 Ž 9 9 . 0 2 1 6 2 - 9
N. Atapour et al.r Brain Research 851 (1999) 148–153
as a filter and only particular types of activity patterns can access the synapses in layer III. By stimulating layer IV this filter is bypassed and LTP can be induced in the absence of GABA A blockers w18x. When using high frequency tetanic stimulation, the priming effect of the initial stimulus pulse facilitates LTP induction w10x. However, the possibility of neocortical LTP induction using PBs has not been investigated yet. Therefore, in the present study we used PBs to test the following: 1. Does the temporal pattern of high frequency stimulation and strength of the priming pulse affect the magnitude of neocortical LTP? 2. Is this effect altered by visual deprivation?
2. Material and methods 2.1. Animals Visual cortical slices were prepared from male and female NMRI rats with ages ranging from 29 to 39 postnatal days. Animals were either normally- ŽCON. or dark-reared ŽDR.. CON animals were reared in a standard environment on a 12:12 h lightrdark cycle and housed in cages with their siblings and parents. DR rats were born and housed in total darkness, except for brief Ž) 5 min total. exposure to dim red light necessary to verify birth and remove from the cage for slicing. 2.2. Slice preparation Animals were anesthetized with ether and were decapitated. Brain was removed and placed into cold Ž28C–48C., oxygenated artificial cerebrospinal fluid ŽACSF, containing in mM: NaCl 124, KCl 4, CaCl 2 2, MgCl 2 2, KH 2 PO4 1.2, NaHCO 3 26, Glucose 10.. A block of the brain including the primary visual cortex ŽArea 17. was placed on a vibroslice. Slices Ž450–500 mm thick. were cut at a 168 angle with respect to the coronal plane. This angle of cut has proven optimal for the preservation of the geniculocortical fibers w34x. Then slices were transferred to an interface type recording chamber and maintained throughout the experiments at the liquidrgas interface with a moistened and oxygenated atmosphere, kept at 32 " 28C. Slices were perfused with ACSF at a flow rate of 2 mlrmin and incubated for 2 h prior to electrophysiological recordings. To allow recordings to be targeted in Area 17, only slices closely matching sections pictured by Paxinos and Watson w27x were used. Only one slice was used from each animal. 2.3. Electrophysiology Field potentials were recorded from layer IIrIII Ž400– 500 mm below the cortical surface. with a glass mi-
149
cropipette filled with NaCl Ž2 M. yielding impedance of 2.0–5.0 M V. A monopolar recording configuration was employed with the slice pool grounded. The signal was amplified using a MEZ-8300 microelectrode amplifier in series with a differential amplifier ŽTektronix, AM 502.. Electrical stimulation was administered via a bipolar stimulating electrode consisting of two teflon-coated stainless steel wires with a tip size of 60 mm driven by a constant current Grass S88 stimulator. The stimulating electrode was placed on the layer IV about 250–500 mm lateral to a line orthogonal to the cortical surface and passing through the recording site. Field potentials of layer IIrIII were evoked by stimulation of layer IV delivered at 10-s intervals. The stimulus test pulses were delivered at two fixed intensities of 20 and 200 mA and pulse width Ž200 ms. was fixed for each slice. Slices that exhibited thresholds greater than 20 mA were considered unhealthy and were not used. Before a tetanus was delivered the average evoked field potentials were required to be stable for 30 min. When variation in field potential amplitude was less than "10% for 30 min, the baseline recordings were considered stable. Before and 30 min after tetanus, field potentials of layer IIrIII were recorded at two fixed intensities. For induction of LTP, a tetanus consisting of eight PBs at 200 mA stimulus intensity was delivered with a PB interval of 10 s. The PBs pattern was one pulse followed 170 ms later by a burst of 10 pulses at 100 Hz. Ten responses were evoked, amplified, digitized Žat 20 kHz. and averaged for each stimulus intensity. To confirm the synaptic nature of field potentials, Ca2q was omitted from ACSF at the end of some of experiments. 2.4. Data analysis The amplitude of population excitatory postsynaptic potential 1 ŽpEPSP1 , from the beginning of the first negative wave to its peak in mV. and pEPSP2 Žfrom the beginning of the second negative wave to its peak in mV. was measured from averaged waveforms before and 30 min after PBs. Then, the amplitude of each component was expressed as a percent of its average amplitude before the PBs at each stimulus intensity. Our criteria for LTP was more than 20% increase and for long-term depression ŽLTD., 20% decrease in pEPSP amplitude relative to baseline that lasted for 30 min at 20 mA stimulus intensity w3x. Other parameters of field potentials were measured as follows. Peak latency of pEPSP1 Žfrom the stimulus artifact to the peak of the first negative wave in ms., peak latency of pEPSP2 Žfrom the stimulus artifact to the peak of the second negative wave in ms., slope of pEPSP1 Žfrom 10% to 90% points of the raising phase of pEPSP1 . and slope of pEPSP2 Žfrom 10% to 90% points of the raising phase of pEPSP2 .. All data are expressed as mean " S.E.M. Unpaired t-test and Pearson’s linear correlation were used for
150
N. Atapour et al.r Brain Research 851 (1999) 148–153
the comparison. Results considered significant at the level of P - 0.05.
3. Results The field potentials elicited in layer IIrIII in response to layer IV stimulation consisted of two major components. Both components were dissolved in low Ca2q ACSF. Therefore, the response components were called pEPSP1 and pEPSP2 , which refer to the first and the second negativity, respectively ŽFig. 1.. In CON slices, pEPSP1 was elicited with mean peak latency of 2.38 " 0.10 ms and pEPSP2 with mean peak latency of 5.31 " 0.15 ms. Different underlying synaptic mechanisms and neurotransmitter systems may be involved in the generation of each component w31x. Therefore, the effects of light deprivation on PBs-induced changes in the amplitude, latency and slope of each component were examined separately. 3.1. Synaptic potentiation The application of PBs to layer IV led to robust potentiation of layer IIrIII field potentials ŽFig. 1.. In CON slices Ž n s 10., PBs had no remarkable effect on the pEPSP1 amplitude except in one slice in which the pEPSP1 amplitude decreased Žy31.90%.. But in half of DR slices Žfour out of eight. PBs led to the significant potentiation of pEPSP1. Mean % increase of amplitude in four mentioned cases of LTP was 30.78 " 3.75 at low stimulus intensity.
Fig. 2. Mean % increase of amplitude of pEPSP2 in CON and DR slices at 20 and 200 mA stimulus intensities. The data shown are mean"S.E.M. U P - 0.05 Žunpaired t-test..
The LTP of pEPSP1 was observed only when low stimulus intensities were used and the degree of potentiation decreased with increasing stimulus intensity. LTD was observed in one DR slice Žy26.98%. and in the other DR slices Žthree out of eight. PBs had no considerable effect. PBs led to the potentiation of pEPSP2 in all slices from both CON and DR rats. CON slices exhibited considerable potentiation, while DR slices showed a much smaller degree of potentiation ŽFig. 2.. Comparison of the mean % increase of pEPSP2 amplitude between CON and DR slices showed that the degree of potentiation was lower in DR slices. This difference was significant at both stimulus intensities Žunpaired t-test, P - 0.05.. 3.2. Slope In the hippocampus, the slope of the field EPSP has been considered to be an indicator of synaptic strength w22x. In hippocampal slices the tetanic stimulation-induced changes in slope and amplitude of pEPSP are in the same direction w10x. To investigate if such relation also exists in neocortical slices, the correlation between changes in amplitude and slope of pEPSPs in both groups and both stimulus intensities were evaluated using Pearson’s linear correlation. No significant correlation was found between the slope and amplitude of each component of field potential. pEPSP1: wŽCON group: 20 mA, r s 0.31, P ) 0.05 and 200 mA, r s y0.30, P ) 0.05., ŽDR group: 20 mA, r s 0.25, P ) 0.05 and 200 mA, r s y0.19, P ) 0.05.x and pEPSP2 : wŽCON group: 20 mA, r s 0.06, P ) 0.05 and 200 mA, r s 0.40, P ) 0.05., ŽDR group, 20 mA, r s y0.48, P ) 0.05, and 200 mA, r s 0.18, P ) 0.05.x. 3.3. Peak latency
Fig. 1. Representative layer IIrIII field potentials of visual cortical slices from CON and DR rats, before and 30 min after PBs at 20 mA stimulus intensity. Each trace is the average of 10 responses.
Based on the intracellular studies of Voronin et al. w33x about the decrease of response latency during LTP and its increase during LTD, we evaluated the peak latency of
N. Atapour et al.r Brain Research 851 (1999) 148–153 Table 1 PBs-induced changes in peak latency of pEPSP1 and pEPSP2 in CON and DR slices Latency changes are shown as decrease Žy., increase Žq. or no change Ž". with respect to the occurrence of LTP, LTD or None. Group pEPSP1 LTP CON DR
pEPSP2 LTD
None
LTP
LTD None
1Ž". 5Ž"., 2Žy., 2Žq. 8Žy. 4Žy. 1Žq. 1Ž"., 2Žq. 5Žy., 3Žq.
pEPSP1 and pEPSP2 after application of PBs. We did not find any relationship between the latency changes of pEPSP1 and the occurrence of LTP or LTD. In the CON group, the latency of pEPSP2 decreased in all cases of LTP, while in the DR group it was seen only in five out of eight cases of LTP. In the three cases of LTP, latency increased ŽTable 1..
4. Discussion The present results show the following: 1. Application of PBs to layer IV of rat visual cortical slices, could effectively induce LTP of layer IIrIII field potentials. In CON slices, it led to selective potentiation of pEPSP2 . 2. Visual deprivation had different effects on PBs-induced LTP. It increased the incidence of LTP of pEPSP1 and decreased the amount of LTP of pEPSP2 . 4.1. Strength of priming and LTP susceptibility In the present study the amplitude of pEPSP2 increased 234.5 " 45.1% with respect to the baseline. Many reports in which the induction of neocortical LTP was attempted using TBS or other types of stimulus paradigm showed that the degree of potentiation of pEPSP reaches 71% or less of the baseline w2,8,18–20,31,35x. A more direct comparison can be made between the present results and that of Kirkwood and Bear w18x. Since in both experiments layer IV has been stimulated, GABA A blockers were not used and the LTP of the second component of field potential was obtained. No significant difference seems to exist in the ACSF composition and the rat primary visual cortex is the site of recording, suggesting that PBs are more effective in neocortical LTP induction compared to other stimulus paradigms. Also, due to the difficulty of LTP induction in the neocortex, most neocortical tetanus parameters cannot induce LTP in all cases w31x. Therefore, the present results support our hypothesis that the presence of the priming pulse and temporal pattern of PBs are very effective in the induction of neocortical LTP. In contrast to neocortex, TBS and PBs affect the hippocampus in a similar manner. Using PBs, the amplitude
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of hippocampal pEPSP potentiated 30.0 " 2.4% w21x, 44.0 " 4.4% w12x and 78.0 " 21.0% w29x of the baseline and TBS led to potentiation of 43.0 " 7.0% w19x or 50.0 " 13.0% w9x of the baseline. One of the major differences between the hippocampus and the neocortex is the complex inhibitory circuitry in the neocortex and synaptic plasticity in neocortex is therefore expected to be greatly influenced by the inhibitory circuitry w18x. pEPSP2 represents the activity of excitatory polysynaptic circuits mediated especially by NMDA receptors w3,31x. pEPSP1 , the monosynaptic component of the field potential, includes a kainaterAMPA and NMDA receptor-mediated potentials w3,31x. The selective potentiation of pEPSP2 suggests that the effects of PBs may be due to its influence on NMDA receptors. The slight participation of NMDA receptors in mediating pEPSP1 supports this assumption. However, clarification of the effects of PBs on NMDA receptors or GABAergic system needs further work. 4.2. PBs-induced changes in slope and latency In the hippocampus, the amplitude of field potential can be considered as a measure of the number of involved cells and indirectly reflects the degree of synchronization of activity while the slope of field potential directly shows the level of synchronization. As shown in this study, plasticity-induced changes in these two parameters are not in the same direction and do not correlate significantly, in contrast to hippocampus. The neocortical network differs in many details from the hippocampal network. The wider dispersion of neurons in the neocortex reduces the efficacy of field effects because of both the smaller voltage gradient and the lack of dense, high resistance pyramidal cell layer w16x. Therefore, due to the complex nature of cortical field potentials, in most cases only relative changes in amplitude are interpreted as change in the amount of transmembranal currents. These differences between the neocortical and hippocampal networks might affect the changes of population response latency during LTP or LTD. Intracellular recording from neocortical and hippocampal neurons has shown that response latency decreases in some cases of LTP and increases in some cases of LTD w33x. This correlation, which shows the possibility of changes in functional state of synapses during LTP or LTD w33x, could not be addressed in neocortical field potentials in this study. 4.3. Effects of Õisual depriÕation on LTP In this study, visual deprivation decreased LTP of pEPSP2 . It is in contrast to the study of Kirkwood et al. w20x on rat visual cortical slices, which showed that visual deprivation increases LTP of layer IIrIII field potentials. Probably, it is due to the difference in the type of tetanic
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stimulation which is also mentioned in the reports of Kirkwood et al. w20x. They indicated that TBS induced LTP of comparable magnitude in slices from CON and DR rats. However, the same number of pulses delivered in 20-Hz bursts caused significant potentiation in slices from DR rats but little synaptic change in CON slices w20x. Since pEPSP2 is especially mediated by NMDA receptors w3,31x, it is suggested that the selective patterns of tetanic stimulations may affect NMDA receptors differently. On the other hand, recent evidences have suggested a modifiable threshold for LTP induction that is dependent on the history of prior synaptic activity. Induction probability and magnitude of LTP and LTD depends on the prevailing level of synaptic activity just prior to tetanic stimulation w1,32x. Therefore, we suggest that the lower magnitude of LTP of pEPSP2 in DR slices, may be due to the higher density of NMDA receptors, which augments prior synaptic activity. Several reports have shown that the density of NMDA receptors are maximal before the maturation of neocortex w13–15x and visual deprivation prevents the developmental decline of NMDA receptors w13x and their mediated responses w7x. However, it is very essential to evaluate role of NMDA receptors using their antagonists. Visual deprivation increased incidence of LTP of pEPSP1. Role of NMDA receptors is not essential in the induction of pEPSP1 w3,31x. Therefore, it seems that probable higher density of NMDA receptors may hardly affect prior synaptic activity and LTP in this component. It is suggested that the participation of other glutamate receptors might increase the incidence of LTP of pEPSP1. Metabotropic glutamate receptors ŽmGluRs. may also be involved in the effect of dark-rearing. Although different studies have shown the influences of dark-rearing on mGluRs, they are not consistent with each other w11,28x. However, the differential effects of PBs on LTP of pEPSP1 and pEPSP2 need future investigation. The effects of visual deprivation on LTP of pEPSP1 were limited to low stimulus intensity. It may be due to activation of inhibitory fibers at high stimulus intensity which coincide temporally with potentiated pEPSP1 w24,30,31x. In conclusion, PBs could be used as an effective tetanic stimulation to study synaptic plasticity in different conditions, such as visually deprived animals in present study. It seems that the effects of visual deprivation also depend on the pattern of high frequency stimulation.
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Research report
Primed-bursts induced long-term potentiation in rat visual cortex: effects of dark-rearing Nafiseh Atapour a
a,b,)
, Hossein Esteky a , Yaghoub Fathollahi c , Farshad Alizadeh Mansouri
a
Department of Physiology, School of Medicine, Shaheed Beheshti UniÕersity of Medical Sciences, Tehran, Iran b Department of Physiology, School of Medicine, Kerman UniÕersity of Medical Sciences, Kerman, Iran c Department of Physiology, School of Medical Sciences, Tarbiat Modarress UniÕersity, Tehran, Iran Accepted 21 September 1999
Abstract Theta burst stimulation ŽTBS. and primed bursts ŽPBs. stimulation are among the effective tetanic stimulations for induction of long-term potentiation ŽLTP. in the hippocampus. Recent studies have indicated that TBS is effective in LTP induction of layer III synapses of neocortex, only if applied to layer IV. However, the possibility of neocortical LTP induction using PBs has not been investigated yet. Sensory deprivation greatly influences the development of neocortex. According to the effect of sensory deprivation on synaptic plasticity of developing neocortex, we studied the induction of LTP by PBs in visual cortical slices of control and dark-reared rats. The results showed that application of PBs to layer IV could effectively induce LTP of layer IIrIII field potentials. These potentials are consisted of two components: pEPSP1 Žpopulation excitatory postsynaptic potential 1. and pEPSP2 . In control slices PBs led to selective potentiation of pEPSP2 . Visual deprivation increased the incidence of LTP of pEPSP1 and decreased the amount of LTP of pEPSP2 . These findings showed that PBs could be used as an effective tetanic stimulation to study the synaptic plasticity in neocortex. The effects of visual deprivation on PBs-induced LTP are consistent with its role in the development of excitatory system in neocortex. q 1999 Published by Elsevier Science B.V. All rights reserved. Keywords: Tetanic stimulation; Brain slice; Plasticity; Field potential; Dark-rearing
1. Introduction The normal development of visual cortex during early postnatal period could be altered by manipulation of visual experience. For example, dark-rearing delays the loss of N-methyl-D-aspartate ŽNMDA. receptor function in kitten w13x and NMDA receptor-mediated currents in rat visual cortex w7x. Also, visual deprivation decreases long-term potentiation ŽLTP. in visual cortical slices of 17- to 21day-old rats w6x and increases it in adult rat neocortex w20x. LTP is a long-lasting increase in synaptic efficacy elicited by brief, high frequency bursts of synaptic activation. Activation of NMDA receptors is essential for the induction of neocortical LTP w4,17x. Different studies on rat neocortex have shown that the activity of NMDA system increases to a maximum during the second and third postnatal weeks and then declines slightly in adulthood w7,14–16,24,26x. Critical period for maximum LTP ) C orresponding author. [email protected]
Fax:
q 98-341-55098;
e-m ail:
induction coincides temporally with a ‘‘developmental window’’ within which activity of NMDA system is enhanced w17,24x. GABAergic system matures gradually during the first postnatal month w23x. During the ‘‘developmental window’’ the GABAergic inhibition is immature w24x. Maturation of GABAergic inhibition decreases the neocortical susceptibility for LTP induction w17x. Slight inhibition of this system has been shown to be essential for the activation of NMDA receptors and neocortical LTP induction w4,5x. The induction of LTP in the neocortex is more difficult than in the hippocampus w31x. Theta burst stimulation ŽTBS. and primed bursts ŽPBs. tetanic stimulation are widely used in the induction of LTP in the hippocampus w9,12,21,25,29x. It has been shown that in the absence of GABA A blockers, TBS can induce LTP in neocortical layer III synapses only if applied to layer IV and not to the white matter w18x. Application of TBS to the white matter could be effective in the neocortex only if GABA A receptors are blocked w18x. According to the Kirkwood and Bear plasticity gate hypothesis, layer IV inhibitory circuits act
0006-8993r99r$ - see front matter q 1999 Published by Elsevier Science B.V. All rights reserved. PII: S 0 0 0 6 - 8 9 9 3 Ž 9 9 . 0 2 1 6 2 - 9
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as a filter and only particular types of activity patterns can access the synapses in layer III. By stimulating layer IV this filter is bypassed and LTP can be induced in the absence of GABA A blockers w18x. When using high frequency tetanic stimulation, the priming effect of the initial stimulus pulse facilitates LTP induction w10x. However, the possibility of neocortical LTP induction using PBs has not been investigated yet. Therefore, in the present study we used PBs to test the following: 1. Does the temporal pattern of high frequency stimulation and strength of the priming pulse affect the magnitude of neocortical LTP? 2. Is this effect altered by visual deprivation?
2. Material and methods 2.1. Animals Visual cortical slices were prepared from male and female NMRI rats with ages ranging from 29 to 39 postnatal days. Animals were either normally- ŽCON. or dark-reared ŽDR.. CON animals were reared in a standard environment on a 12:12 h lightrdark cycle and housed in cages with their siblings and parents. DR rats were born and housed in total darkness, except for brief Ž) 5 min total. exposure to dim red light necessary to verify birth and remove from the cage for slicing. 2.2. Slice preparation Animals were anesthetized with ether and were decapitated. Brain was removed and placed into cold Ž28C–48C., oxygenated artificial cerebrospinal fluid ŽACSF, containing in mM: NaCl 124, KCl 4, CaCl 2 2, MgCl 2 2, KH 2 PO4 1.2, NaHCO 3 26, Glucose 10.. A block of the brain including the primary visual cortex ŽArea 17. was placed on a vibroslice. Slices Ž450–500 mm thick. were cut at a 168 angle with respect to the coronal plane. This angle of cut has proven optimal for the preservation of the geniculocortical fibers w34x. Then slices were transferred to an interface type recording chamber and maintained throughout the experiments at the liquidrgas interface with a moistened and oxygenated atmosphere, kept at 32 " 28C. Slices were perfused with ACSF at a flow rate of 2 mlrmin and incubated for 2 h prior to electrophysiological recordings. To allow recordings to be targeted in Area 17, only slices closely matching sections pictured by Paxinos and Watson w27x were used. Only one slice was used from each animal. 2.3. Electrophysiology Field potentials were recorded from layer IIrIII Ž400– 500 mm below the cortical surface. with a glass mi-
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cropipette filled with NaCl Ž2 M. yielding impedance of 2.0–5.0 M V. A monopolar recording configuration was employed with the slice pool grounded. The signal was amplified using a MEZ-8300 microelectrode amplifier in series with a differential amplifier ŽTektronix, AM 502.. Electrical stimulation was administered via a bipolar stimulating electrode consisting of two teflon-coated stainless steel wires with a tip size of 60 mm driven by a constant current Grass S88 stimulator. The stimulating electrode was placed on the layer IV about 250–500 mm lateral to a line orthogonal to the cortical surface and passing through the recording site. Field potentials of layer IIrIII were evoked by stimulation of layer IV delivered at 10-s intervals. The stimulus test pulses were delivered at two fixed intensities of 20 and 200 mA and pulse width Ž200 ms. was fixed for each slice. Slices that exhibited thresholds greater than 20 mA were considered unhealthy and were not used. Before a tetanus was delivered the average evoked field potentials were required to be stable for 30 min. When variation in field potential amplitude was less than "10% for 30 min, the baseline recordings were considered stable. Before and 30 min after tetanus, field potentials of layer IIrIII were recorded at two fixed intensities. For induction of LTP, a tetanus consisting of eight PBs at 200 mA stimulus intensity was delivered with a PB interval of 10 s. The PBs pattern was one pulse followed 170 ms later by a burst of 10 pulses at 100 Hz. Ten responses were evoked, amplified, digitized Žat 20 kHz. and averaged for each stimulus intensity. To confirm the synaptic nature of field potentials, Ca2q was omitted from ACSF at the end of some of experiments. 2.4. Data analysis The amplitude of population excitatory postsynaptic potential 1 ŽpEPSP1 , from the beginning of the first negative wave to its peak in mV. and pEPSP2 Žfrom the beginning of the second negative wave to its peak in mV. was measured from averaged waveforms before and 30 min after PBs. Then, the amplitude of each component was expressed as a percent of its average amplitude before the PBs at each stimulus intensity. Our criteria for LTP was more than 20% increase and for long-term depression ŽLTD., 20% decrease in pEPSP amplitude relative to baseline that lasted for 30 min at 20 mA stimulus intensity w3x. Other parameters of field potentials were measured as follows. Peak latency of pEPSP1 Žfrom the stimulus artifact to the peak of the first negative wave in ms., peak latency of pEPSP2 Žfrom the stimulus artifact to the peak of the second negative wave in ms., slope of pEPSP1 Žfrom 10% to 90% points of the raising phase of pEPSP1 . and slope of pEPSP2 Žfrom 10% to 90% points of the raising phase of pEPSP2 .. All data are expressed as mean " S.E.M. Unpaired t-test and Pearson’s linear correlation were used for
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the comparison. Results considered significant at the level of P - 0.05.
3. Results The field potentials elicited in layer IIrIII in response to layer IV stimulation consisted of two major components. Both components were dissolved in low Ca2q ACSF. Therefore, the response components were called pEPSP1 and pEPSP2 , which refer to the first and the second negativity, respectively ŽFig. 1.. In CON slices, pEPSP1 was elicited with mean peak latency of 2.38 " 0.10 ms and pEPSP2 with mean peak latency of 5.31 " 0.15 ms. Different underlying synaptic mechanisms and neurotransmitter systems may be involved in the generation of each component w31x. Therefore, the effects of light deprivation on PBs-induced changes in the amplitude, latency and slope of each component were examined separately. 3.1. Synaptic potentiation The application of PBs to layer IV led to robust potentiation of layer IIrIII field potentials ŽFig. 1.. In CON slices Ž n s 10., PBs had no remarkable effect on the pEPSP1 amplitude except in one slice in which the pEPSP1 amplitude decreased Žy31.90%.. But in half of DR slices Žfour out of eight. PBs led to the significant potentiation of pEPSP1. Mean % increase of amplitude in four mentioned cases of LTP was 30.78 " 3.75 at low stimulus intensity.
Fig. 2. Mean % increase of amplitude of pEPSP2 in CON and DR slices at 20 and 200 mA stimulus intensities. The data shown are mean"S.E.M. U P - 0.05 Žunpaired t-test..
The LTP of pEPSP1 was observed only when low stimulus intensities were used and the degree of potentiation decreased with increasing stimulus intensity. LTD was observed in one DR slice Žy26.98%. and in the other DR slices Žthree out of eight. PBs had no considerable effect. PBs led to the potentiation of pEPSP2 in all slices from both CON and DR rats. CON slices exhibited considerable potentiation, while DR slices showed a much smaller degree of potentiation ŽFig. 2.. Comparison of the mean % increase of pEPSP2 amplitude between CON and DR slices showed that the degree of potentiation was lower in DR slices. This difference was significant at both stimulus intensities Žunpaired t-test, P - 0.05.. 3.2. Slope In the hippocampus, the slope of the field EPSP has been considered to be an indicator of synaptic strength w22x. In hippocampal slices the tetanic stimulation-induced changes in slope and amplitude of pEPSP are in the same direction w10x. To investigate if such relation also exists in neocortical slices, the correlation between changes in amplitude and slope of pEPSPs in both groups and both stimulus intensities were evaluated using Pearson’s linear correlation. No significant correlation was found between the slope and amplitude of each component of field potential. pEPSP1: wŽCON group: 20 mA, r s 0.31, P ) 0.05 and 200 mA, r s y0.30, P ) 0.05., ŽDR group: 20 mA, r s 0.25, P ) 0.05 and 200 mA, r s y0.19, P ) 0.05.x and pEPSP2 : wŽCON group: 20 mA, r s 0.06, P ) 0.05 and 200 mA, r s 0.40, P ) 0.05., ŽDR group, 20 mA, r s y0.48, P ) 0.05, and 200 mA, r s 0.18, P ) 0.05.x. 3.3. Peak latency
Fig. 1. Representative layer IIrIII field potentials of visual cortical slices from CON and DR rats, before and 30 min after PBs at 20 mA stimulus intensity. Each trace is the average of 10 responses.
Based on the intracellular studies of Voronin et al. w33x about the decrease of response latency during LTP and its increase during LTD, we evaluated the peak latency of
N. Atapour et al.r Brain Research 851 (1999) 148–153 Table 1 PBs-induced changes in peak latency of pEPSP1 and pEPSP2 in CON and DR slices Latency changes are shown as decrease Žy., increase Žq. or no change Ž". with respect to the occurrence of LTP, LTD or None. Group pEPSP1 LTP CON DR
pEPSP2 LTD
None
LTP
LTD None
1Ž". 5Ž"., 2Žy., 2Žq. 8Žy. 4Žy. 1Žq. 1Ž"., 2Žq. 5Žy., 3Žq.
pEPSP1 and pEPSP2 after application of PBs. We did not find any relationship between the latency changes of pEPSP1 and the occurrence of LTP or LTD. In the CON group, the latency of pEPSP2 decreased in all cases of LTP, while in the DR group it was seen only in five out of eight cases of LTP. In the three cases of LTP, latency increased ŽTable 1..
4. Discussion The present results show the following: 1. Application of PBs to layer IV of rat visual cortical slices, could effectively induce LTP of layer IIrIII field potentials. In CON slices, it led to selective potentiation of pEPSP2 . 2. Visual deprivation had different effects on PBs-induced LTP. It increased the incidence of LTP of pEPSP1 and decreased the amount of LTP of pEPSP2 . 4.1. Strength of priming and LTP susceptibility In the present study the amplitude of pEPSP2 increased 234.5 " 45.1% with respect to the baseline. Many reports in which the induction of neocortical LTP was attempted using TBS or other types of stimulus paradigm showed that the degree of potentiation of pEPSP reaches 71% or less of the baseline w2,8,18–20,31,35x. A more direct comparison can be made between the present results and that of Kirkwood and Bear w18x. Since in both experiments layer IV has been stimulated, GABA A blockers were not used and the LTP of the second component of field potential was obtained. No significant difference seems to exist in the ACSF composition and the rat primary visual cortex is the site of recording, suggesting that PBs are more effective in neocortical LTP induction compared to other stimulus paradigms. Also, due to the difficulty of LTP induction in the neocortex, most neocortical tetanus parameters cannot induce LTP in all cases w31x. Therefore, the present results support our hypothesis that the presence of the priming pulse and temporal pattern of PBs are very effective in the induction of neocortical LTP. In contrast to neocortex, TBS and PBs affect the hippocampus in a similar manner. Using PBs, the amplitude
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of hippocampal pEPSP potentiated 30.0 " 2.4% w21x, 44.0 " 4.4% w12x and 78.0 " 21.0% w29x of the baseline and TBS led to potentiation of 43.0 " 7.0% w19x or 50.0 " 13.0% w9x of the baseline. One of the major differences between the hippocampus and the neocortex is the complex inhibitory circuitry in the neocortex and synaptic plasticity in neocortex is therefore expected to be greatly influenced by the inhibitory circuitry w18x. pEPSP2 represents the activity of excitatory polysynaptic circuits mediated especially by NMDA receptors w3,31x. pEPSP1 , the monosynaptic component of the field potential, includes a kainaterAMPA and NMDA receptor-mediated potentials w3,31x. The selective potentiation of pEPSP2 suggests that the effects of PBs may be due to its influence on NMDA receptors. The slight participation of NMDA receptors in mediating pEPSP1 supports this assumption. However, clarification of the effects of PBs on NMDA receptors or GABAergic system needs further work. 4.2. PBs-induced changes in slope and latency In the hippocampus, the amplitude of field potential can be considered as a measure of the number of involved cells and indirectly reflects the degree of synchronization of activity while the slope of field potential directly shows the level of synchronization. As shown in this study, plasticity-induced changes in these two parameters are not in the same direction and do not correlate significantly, in contrast to hippocampus. The neocortical network differs in many details from the hippocampal network. The wider dispersion of neurons in the neocortex reduces the efficacy of field effects because of both the smaller voltage gradient and the lack of dense, high resistance pyramidal cell layer w16x. Therefore, due to the complex nature of cortical field potentials, in most cases only relative changes in amplitude are interpreted as change in the amount of transmembranal currents. These differences between the neocortical and hippocampal networks might affect the changes of population response latency during LTP or LTD. Intracellular recording from neocortical and hippocampal neurons has shown that response latency decreases in some cases of LTP and increases in some cases of LTD w33x. This correlation, which shows the possibility of changes in functional state of synapses during LTP or LTD w33x, could not be addressed in neocortical field potentials in this study. 4.3. Effects of Õisual depriÕation on LTP In this study, visual deprivation decreased LTP of pEPSP2 . It is in contrast to the study of Kirkwood et al. w20x on rat visual cortical slices, which showed that visual deprivation increases LTP of layer IIrIII field potentials. Probably, it is due to the difference in the type of tetanic
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stimulation which is also mentioned in the reports of Kirkwood et al. w20x. They indicated that TBS induced LTP of comparable magnitude in slices from CON and DR rats. However, the same number of pulses delivered in 20-Hz bursts caused significant potentiation in slices from DR rats but little synaptic change in CON slices w20x. Since pEPSP2 is especially mediated by NMDA receptors w3,31x, it is suggested that the selective patterns of tetanic stimulations may affect NMDA receptors differently. On the other hand, recent evidences have suggested a modifiable threshold for LTP induction that is dependent on the history of prior synaptic activity. Induction probability and magnitude of LTP and LTD depends on the prevailing level of synaptic activity just prior to tetanic stimulation w1,32x. Therefore, we suggest that the lower magnitude of LTP of pEPSP2 in DR slices, may be due to the higher density of NMDA receptors, which augments prior synaptic activity. Several reports have shown that the density of NMDA receptors are maximal before the maturation of neocortex w13–15x and visual deprivation prevents the developmental decline of NMDA receptors w13x and their mediated responses w7x. However, it is very essential to evaluate role of NMDA receptors using their antagonists. Visual deprivation increased incidence of LTP of pEPSP1. Role of NMDA receptors is not essential in the induction of pEPSP1 w3,31x. Therefore, it seems that probable higher density of NMDA receptors may hardly affect prior synaptic activity and LTP in this component. It is suggested that the participation of other glutamate receptors might increase the incidence of LTP of pEPSP1. Metabotropic glutamate receptors ŽmGluRs. may also be involved in the effect of dark-rearing. Although different studies have shown the influences of dark-rearing on mGluRs, they are not consistent with each other w11,28x. However, the differential effects of PBs on LTP of pEPSP1 and pEPSP2 need future investigation. The effects of visual deprivation on LTP of pEPSP1 were limited to low stimulus intensity. It may be due to activation of inhibitory fibers at high stimulus intensity which coincide temporally with potentiated pEPSP1 w24,30,31x. In conclusion, PBs could be used as an effective tetanic stimulation to study synaptic plasticity in different conditions, such as visually deprived animals in present study. It seems that the effects of visual deprivation also depend on the pattern of high frequency stimulation.
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