Thoracic dorsal funicular lesions affect the bouton patterns on, and diameters of, layer VB pyramidal cell somata in rat hindlimb cortex

Abstract

The effect of spinal dorsal funicular lesions (T 12) upon the frequency of boutons on, and diameters of the somata of pyramidal cells in layer VB of hindlimb cortex was studied. Adult rats sustained bilateral damage to either the dorsal column (DC, n = 10) alone or DC combined with the corticospinal tract (CS) (DC + CS, n = 34) and were utilized 1, 2, 3, 7, 14, 30, 45, 60, 90, or 120 days postoperatively (DPO). Neurons randomly sampled from 44 lesioned and 13 unoperated cases were analyzed for the number of silver-impregnated boutons (Rasmussen method) on the circumference of the soma as well as diameters of the soma, nucleus, and nucleolus. Analyses of variance comparing across lesioned and normal groups were significant for bouton counts on the soma (P less than 0.01), and diameters (long axis) of somata (P less than 0.01) and their nuclei (P less than 0.05). Both lesioned groups exhibited significant decreases from normal for these latter three parameters. With respect to survival time for the DC + CS-lesioned animals we noted the following: (1) Bouton counts on the soma significantly decreased below normal between 1 and 60 DPO; this decrease was most dramatic during the first three days postlesion. (2) Somal diameter (long axis) significantly decreased below normal between 2 and 120 DPO (except at 14 and 90 DPO). (3) Nuclear diameter (long axis) significantly decreased below normal only at 90 DPO. (4) Bouton counts on somata of neurons in layers VB and IV [Ganchrow and Bernstein, 1981] of hindlimb cortex correlated negatively and significantly across 120 postlesion days. The rapid shrinkage and reduced afferentation of layer VB somata during the first week following DC + CS lesions suggest initial, retrograde reactions to CS axotomy. Since bouton counts on layer VB somata were significantly less (P less than 0.05) in DC- than DC + CS-lesioned rats, it is hypothesized that CS axotomy regulated a set-point for increased afferentation which was maintained on the shrunken somata between 7 and 120 DPO.

Somatosensory cortical atrophy after spinal cord injury: A voxel-based morphometry study

“…8 Several similar studies suggest that in addition to this degeneration, these cells may persist, but in an atrophic state for some period after trauma. 1,2 In the current study, however, no atrophy was found in M1 or other motor area. The presence of an extensive array of collateral connections within M1 and connections between M1 and higher order motor areas may maintain cellular activity in the motor system, possibly reducing or preventing corticospinal neuronal atrophy after axonal injury.…”

Unexpected Survival of Neurons of Origin of the Pyramidal Tract after Spinal Cord Injury

“…Although there was no evidence of axon degeneration in the pyramid following SCI, previous studies have reported atrophy and shrinkage of the cell bodies of cortical motoneurons (Holmes and May, 1909; Lassek, 1942; Kalil and Schneider, 1975; Barron and Dentinger, 1979; Ganchrow and Bernstein, 1985; Ramirez and Kalil, 1985; Barron et al, 1988; Merline and Kalil, 1990; Tseng and Prince, 1996). Accordingly, it was of interest to determine whether it was possible to detect atrophy of CST axons in the pyramid.…”

“…Numerous studies have addressed this question by assessing changes in the motor cortex following injury, with conclusions ranging from no cell death to extensive retrograde degeneration. Assessments have included counts of neurons in the cortex (Feringa and Vahlsing, 1985; Giehl and Tetzlaff, 1996; Hammond et al, 1999; Bonatz et al, 2000; Hains et al, 2003; Klapka et al, 2005), changes in gene expression in the cell bodies (Kost-Mikucki and Oblinger, 1991; Mikucki and Oblinger, 1991; Kost and Oblinger, 1993; Mason et al, 2003), changes in forelimb representation (Schmidlin et al, 2004; Schmidlin et al, 2005), assessment of motor responses after stimulation in the cortex (Piecharka et al, 2005), shrinkage of the cell bodies (Holmes and May, 1909; Kalil and Schneider, 1975; Ganchrow and Bernstein, 1985; Merline and Kalil, 1990; Wannier et al, 2005) chromatolysis (Holmes and May, 1909; Lassek, 1942; Bodian, 1946), and activation of cell death markers (Hains et al, 2003; Lee et al, 2004). There have also been reports of no response to injury (Mason et al, 2003; Crawley et al, 2004).…”

A reassessment of whether cortical motor neurons die following spinal cord injury

“…All such studies have focused on the motor cortex itself, using a variety of measures including: quantification of cortical neuron numbers (Bonatz et al, 2000; Feringa and Vahlsing, 1985; Feringa et al, 1983; Giehl and Tetzlaff, 1996; Hains et al, 2003; Hammond et al, 1999; Klapka et al, 2005; Sasaki et al, 2006), activation of cell death markers (Hains et al, 2003; Lee et al, 2004; Sasaki et al, 2006), changes in gene expression (Higo et al, 2009; Kost-Mikucki and Oblinger, 1991; Kost and Oblinger, 1993; Mason et al, 2003; Mikucki and Oblinger, 1991), changes in cortical representation (Jurkiewicz et al, 2007; Mikulis et al, 2002; Schmidlin et al, 2004, 2005) or cortical volume and tractography (Wrigley et al, 2009), changes in motor responses after stimulation in the cortex (Piecharka et al, 2005; Schmidlin et al, 2005), cell shrinkage (Beaud et al, 2008; Brock et al, 2010; Ganchrow and Bernstein, 1985; Holmes and May, 1909; Kalil and Schneider, 1975; Merline and Kalil, 1990; Ramirez and Kalil, 1985; Tseng and Prince, 1996; Wannier et al, 2005), and chromatolysis (Barron and Dentinger, 1979; Holmes and May, 1909; Lassek, 1942; Levin and Bradford, 1938). A few studies have reported no response to injury (Crawley et al, 2004; Mason et al, 2003; McBride et al, 1990).…”

“…The question has been addressed in a wide range of animal models including rats (Barron et al, 1988; Bonatz et al, 2000; Brock et al, 2010; Feringa and Vahlsing, 1985; Feringa et al, 1983; Ganchrow and Bernstein, 1985; Giehl and Tetzlaff, 1996; Hains et al, 2003; Hammond et al, 1999; Klapka et al, 2005; Lee et al, 2004; Mason et al, 2003; McBride et al, 1990; Piecharka et al, 2005; Sasaki et al, 2006; Tseng and Prince, 1996), hamsters (Kalil and Schneider, 1975; Kost-Mikucki and Oblinger, 1991; Kost and Oblinger, 1993; Merline and Kalil, 1990; Mikucki and Oblinger, 1991; Ramirez and Kalil, 1985), cats (Barron and Dentinger, 1979), dogs (Holmes and May, 1909), monkeys (Beaud et al, 2008; Brock et al, 2010; Higo et al, 2009; Holmes and May, 1909; Lassek, 1942; Levin and Bradford, 1938; Schmidlin et al, 2005; Schmidlin et al, 2004; Wannier et al, 2005), and humans (Crawley et al, 2004; Holmes and May, 1909; Jurkiewicz et al, 2007; Mikulis et al, 2002; Wrigley et al, 2009). …”