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Increased cortical responses to forepaw stimuli immediately after peripheral deafferentation of hindpaw inputs

View Article: PubMed Central - PubMed

ABSTRACT

Both central and peripheral injuries of the nervous system induce dramatic reorganization of the primary somatosensory cortex. We recently showed that spinal cord injuries at thoracic level in anesthetized rats can immediately increase the responses evoked in the forepaw cortex by forepaw stimuli (above the level of the lesion), suggesting that the immediate cortical reorganization after deafferentation can extend across cortical representations of different paws. Here we show that a complete deafferentation of inputs from the hindpaw induced by injury or pharmacological block of the peripheral nerves in anesthetized rats also increases the responses evoked in the forepaw cortex by forepaw stimuli. This increase of cortical responses after peripheral deafferentation is not associated with gross alterations in the state of cortical spontaneous activity. The results of the present study, together with our previous works on spinal cord injury, suggest that the forepaw somatosensory cortex is critically involved in the reorganization that starts immediately after central or peripheral deafferentation of hindpaw inputs.

No MeSH data available.


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Experimental protocol and evoked responses.(A) Extracellular recordings were made in the forepaw (FP) and hindpaw (HP) representations of the primary somatosensory cortex (Cx) in urethane-anaesthetized rats. Peripheral nerve injury or pharmacological block was performed to both the saphenous and sciatic nerves. (B) We studied both the spontaneous activity and the responses evoked by electrical stimuli delivered to the hindpaw and forepaw at high intensity (5 mA) before (P0: control protocol with intact animal) and after deafferentation at three different time points (P1, P2 and P3: 10-20 min, 1 hour and 2 hours after deafferentation respectively). The experiment was performed in three groups of animals: animals that received injury of the peripheral nerves (black), animals that received pharmacological blockade of the peripheral nerves (dark gray), sham animals with intact nerves (light gray). (C) Grand average of local field potential (LFP) responses evoked by high intensity (5 mA) stimuli delivered either to the contralateral forepaw (left: forepaw cortex; center: hindpaw cortex, enlarged in the inset) or hindpaw (right: hindpaw cortex) before (P0: black) and after peripheral nerve injury, (P1: dark grey; P3: light grey). (D) Left: evolution of the amplitude of the responses evoked in forepaw cortex by forepaw stimuli in the different group of animals (peripheral nerve injury: black; peripheral nerve block: dark grey; sham: light grey) over time (P1, P2 and P3). *:p<0.05; **:p<0.01. Right: Corresponding variability between animals. Note: the values of the evoked responses shown in Figure 1D are normalized in relation to value of the response in P0 (one subject in the injury group with very high values was excluded from the variability plot but included in the average and in the analyses). The responses evoked in the forepaw cortex by forepaw stimuli significantly increased after peripheral deafferentation of hindpaw inputs.
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f1: Experimental protocol and evoked responses.(A) Extracellular recordings were made in the forepaw (FP) and hindpaw (HP) representations of the primary somatosensory cortex (Cx) in urethane-anaesthetized rats. Peripheral nerve injury or pharmacological block was performed to both the saphenous and sciatic nerves. (B) We studied both the spontaneous activity and the responses evoked by electrical stimuli delivered to the hindpaw and forepaw at high intensity (5 mA) before (P0: control protocol with intact animal) and after deafferentation at three different time points (P1, P2 and P3: 10-20 min, 1 hour and 2 hours after deafferentation respectively). The experiment was performed in three groups of animals: animals that received injury of the peripheral nerves (black), animals that received pharmacological blockade of the peripheral nerves (dark gray), sham animals with intact nerves (light gray). (C) Grand average of local field potential (LFP) responses evoked by high intensity (5 mA) stimuli delivered either to the contralateral forepaw (left: forepaw cortex; center: hindpaw cortex, enlarged in the inset) or hindpaw (right: hindpaw cortex) before (P0: black) and after peripheral nerve injury, (P1: dark grey; P3: light grey). (D) Left: evolution of the amplitude of the responses evoked in forepaw cortex by forepaw stimuli in the different group of animals (peripheral nerve injury: black; peripheral nerve block: dark grey; sham: light grey) over time (P1, P2 and P3). *:p<0.05; **:p<0.01. Right: Corresponding variability between animals. Note: the values of the evoked responses shown in Figure 1D are normalized in relation to value of the response in P0 (one subject in the injury group with very high values was excluded from the variability plot but included in the average and in the analyses). The responses evoked in the forepaw cortex by forepaw stimuli significantly increased after peripheral deafferentation of hindpaw inputs.

Mentions: To test this hypothesis we performed experiments in 29 male anesthetized rats, which were divided in three groups (Fig. 1A,B): (1) animals that received a peripheral injury to the hindpaw, consisting of a complete section of both the sciatic and saphenous nerves (n = 11); (2) animals that received a pharmacological block of the same peripheral nerves by injection of lidocaine (n = 10); (3) sham animals (n = 8). We specifically investigated the possible changes in the responses evoked in the forepaw cortex17 by electrical stimuli delivered to the forepaw, as well as possible changes in cortical spontaneous activity, within two hours after injury or pharmacological block of the peripheral nerves in the hindpaw.


Increased cortical responses to forepaw stimuli immediately after peripheral deafferentation of hindpaw inputs
Experimental protocol and evoked responses.(A) Extracellular recordings were made in the forepaw (FP) and hindpaw (HP) representations of the primary somatosensory cortex (Cx) in urethane-anaesthetized rats. Peripheral nerve injury or pharmacological block was performed to both the saphenous and sciatic nerves. (B) We studied both the spontaneous activity and the responses evoked by electrical stimuli delivered to the hindpaw and forepaw at high intensity (5 mA) before (P0: control protocol with intact animal) and after deafferentation at three different time points (P1, P2 and P3: 10-20 min, 1 hour and 2 hours after deafferentation respectively). The experiment was performed in three groups of animals: animals that received injury of the peripheral nerves (black), animals that received pharmacological blockade of the peripheral nerves (dark gray), sham animals with intact nerves (light gray). (C) Grand average of local field potential (LFP) responses evoked by high intensity (5 mA) stimuli delivered either to the contralateral forepaw (left: forepaw cortex; center: hindpaw cortex, enlarged in the inset) or hindpaw (right: hindpaw cortex) before (P0: black) and after peripheral nerve injury, (P1: dark grey; P3: light grey). (D) Left: evolution of the amplitude of the responses evoked in forepaw cortex by forepaw stimuli in the different group of animals (peripheral nerve injury: black; peripheral nerve block: dark grey; sham: light grey) over time (P1, P2 and P3). *:p<0.05; **:p<0.01. Right: Corresponding variability between animals. Note: the values of the evoked responses shown in Figure 1D are normalized in relation to value of the response in P0 (one subject in the injury group with very high values was excluded from the variability plot but included in the average and in the analyses). The responses evoked in the forepaw cortex by forepaw stimuli significantly increased after peripheral deafferentation of hindpaw inputs.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5384276&req=5

f1: Experimental protocol and evoked responses.(A) Extracellular recordings were made in the forepaw (FP) and hindpaw (HP) representations of the primary somatosensory cortex (Cx) in urethane-anaesthetized rats. Peripheral nerve injury or pharmacological block was performed to both the saphenous and sciatic nerves. (B) We studied both the spontaneous activity and the responses evoked by electrical stimuli delivered to the hindpaw and forepaw at high intensity (5 mA) before (P0: control protocol with intact animal) and after deafferentation at three different time points (P1, P2 and P3: 10-20 min, 1 hour and 2 hours after deafferentation respectively). The experiment was performed in three groups of animals: animals that received injury of the peripheral nerves (black), animals that received pharmacological blockade of the peripheral nerves (dark gray), sham animals with intact nerves (light gray). (C) Grand average of local field potential (LFP) responses evoked by high intensity (5 mA) stimuli delivered either to the contralateral forepaw (left: forepaw cortex; center: hindpaw cortex, enlarged in the inset) or hindpaw (right: hindpaw cortex) before (P0: black) and after peripheral nerve injury, (P1: dark grey; P3: light grey). (D) Left: evolution of the amplitude of the responses evoked in forepaw cortex by forepaw stimuli in the different group of animals (peripheral nerve injury: black; peripheral nerve block: dark grey; sham: light grey) over time (P1, P2 and P3). *:p<0.05; **:p<0.01. Right: Corresponding variability between animals. Note: the values of the evoked responses shown in Figure 1D are normalized in relation to value of the response in P0 (one subject in the injury group with very high values was excluded from the variability plot but included in the average and in the analyses). The responses evoked in the forepaw cortex by forepaw stimuli significantly increased after peripheral deafferentation of hindpaw inputs.
Mentions: To test this hypothesis we performed experiments in 29 male anesthetized rats, which were divided in three groups (Fig. 1A,B): (1) animals that received a peripheral injury to the hindpaw, consisting of a complete section of both the sciatic and saphenous nerves (n = 11); (2) animals that received a pharmacological block of the same peripheral nerves by injection of lidocaine (n = 10); (3) sham animals (n = 8). We specifically investigated the possible changes in the responses evoked in the forepaw cortex17 by electrical stimuli delivered to the forepaw, as well as possible changes in cortical spontaneous activity, within two hours after injury or pharmacological block of the peripheral nerves in the hindpaw.

View Article: PubMed Central - PubMed

ABSTRACT

Both central and peripheral injuries of the nervous system induce dramatic reorganization of the primary somatosensory cortex. We recently showed that spinal cord injuries at thoracic level in anesthetized rats can immediately increase the responses evoked in the forepaw cortex by forepaw stimuli (above the level of the lesion), suggesting that the immediate cortical reorganization after deafferentation can extend across cortical representations of different paws. Here we show that a complete deafferentation of inputs from the hindpaw induced by injury or pharmacological block of the peripheral nerves in anesthetized rats also increases the responses evoked in the forepaw cortex by forepaw stimuli. This increase of cortical responses after peripheral deafferentation is not associated with gross alterations in the state of cortical spontaneous activity. The results of the present study, together with our previous works on spinal cord injury, suggest that the forepaw somatosensory cortex is critically involved in the reorganization that starts immediately after central or peripheral deafferentation of hindpaw inputs.

No MeSH data available.


Related in: MedlinePlus