doi: 10.1093/cercor/bhn236. Epub 2009 Jan 15.
Resection of the medial temporal lobe disconnects the rostral superior temporal gyrus from some of its projection targets in the frontal lobe and thalamus
Affiliations
- PMID:19150921
- PMCID: PMC2722427
- DOI: 10.1093/cercor/bhn236
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Resection of the medial temporal lobe disconnects the rostral superior temporal gyrus from some of its projection targets in the frontal lobe and thalamus
Monica Muñoz et al. Cereb Cortex.2009 Sep.
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Abstract
Auditory memory in the monkey does not appear to extend beyond the limits of working memory. It is therefore surprising that this ability is impaired by medial temporal lobe (MTL) resections, because such lesions spare working memory in other sensory modalities. To determine whether MTL ablations might have caused the auditory deficit through inadvertent transection of superior temporal gyrus (STG) projections to its downstream targets, and, if so, which targets might have been compromised, we injected anterograde tracer (biotinylated dextran amine) in the STG of both the normal and MTL-lesioned hemispheres of split-brain monkeys. Interhemispheric comparison of label failed to show any effect of the MTL ablation on efferents from caudal STG, which projects to the inferior prefrontal convexity. However, the ablation did consistently interrupt the normally dense projections from rostral STG to both the ventral medial prefrontal cortex and medial thalamic nuclei. The findings support the possibility that the auditory working memory deficit after MTL ablation is due to transection of downstream auditory projections, and indicate that the candidate structures for mediating auditory working memory are the ventral medial prefrontal cortical areas, the medial thalamus, or both.
Figures
Intended extent of anterograde tracer injections (dark gray areas) in the STG of the rhesus monkey, illustrated on lateral views of the left hemisphere and on coronal sections that also depict a unilateral MTL removal on the right hemisphere. (a) Intended injections in rSTG, with “opened” lateral and superior temporal sulci shown in blue. (b) Intended injections in caudal STG shown with “opened” lateral sulcus in blue. Numerals preceded by + refer to approximate coronal levels anterior to the interaural plane. la, lateral sulcus; Ipa, superior temporal cortical area Ipa; ots, occipitotemporal sulcus; Pal, insula, parainsular division; rh, rhinal sulcus; PIR, piriform cortex; RM, rostral medial auditory belt area; tma, anterior middle temporal sulcus; tmp, posterior medial temporal suclus; TF, medial temporal cortical area TF; TH, medial temporal cortical area TH; Tpt, temporoparietal area; ts, superior temporal sulcus; 6, 8, 9, 10, 11, 12, 13, 14, 24, 25, 28, 32, 35, 36, 45, 46, Brodmann’s cytoarchitectonic areas; 36p, temporal pole division of Brodman's area 36; A1, auditory core area A1; AL, anterior lateral auditory belt area; ML, middle lateral auditory belt area; MM, middle medial auditory belt area; PGa, superior temporal gyrus area; PGa, R, auditory core area R; RT, auditory core area RT; RTL, rostrotemporal lateral auditory belt area, RTM; rostrotemporal medial auditory belt area; TAa, superior temporal gyrus area TAa; TE, inferior temporal gyrus area TE; TPO, superior temporal gyrus area TPO; Ts1, superior temporal gyrus area Ts1; Ts2, superior temporal gyrus area Ts2; Ts3 superior temporal gyrus area Ts3; V, temporal horn of the lateral ventricle.
(a,b) Series of rostral (top) to caudal (bottom) coronal sections from cases M1 and M2 (A) and from cases M3 and M4 (b) illustrating the extents of the bilateral tracer injections in gray, as well as the unilateral MTL removals and forebrain commissurotomies. Note that the MTL removal was on the left in cases M1 and M2 and on the right in the others. Numerals preceded by + refer to approximate coronal levels anterior to the interaural plane. See Figure 1 for abbreviations.
(a,b) Series of rostral (top) to caudal (bottom) coronal sections from cases M1 and M2 (A) and from cases M3 and M4 (b) illustrating the extents of the bilateral tracer injections in gray, as well as the unilateral MTL removals and forebrain commissurotomies. Note that the MTL removal was on the left in cases M1 and M2 and on the right in the others. Numerals preceded by + refer to approximate coronal levels anterior to the interaural plane. See Figure 1 for abbreviations.
Photomicrographs of coronal sections illustrating the actual BDA injection areas in rostral (case M3) and caudal (case M4) STG. Scale bar: 1.4 cm. See Figure 1 for abbreviations.
Lateral surface view and coronal sections (a–l) illustrating anterograde tracer injections (dark gray) in rSTG, with “opened” lateral and superior temporal sulci shown in blue, and resulting fiber and terminal label in case M2. In the intact right hemisphere, labeled efferent fibers from the injected STG region joined 3 major pathways: One coursed through the uncinate fasciculus (h) and led to dense terminal label in the ventral medial frontal cortex (a-g), whereas a second and third followed the ventral amygdalofugal (i,j) and ventral striatum pathways (k,l), leading to dense terminal label in the medial thalamus. In the hemisphere with the MTL removal, all 3 efferent pathways were interrupted resulting in substantially less dense label in these 2 target areas. A, amygdala; 13, 14, 24, 25, 32 Brodman's cytoarchitectonic areas; ai, inferior arcuate sulcus; as, superior arcuate sulcus; p, principal sulcus; PAll, frontal periallocortical area; Pro, proisocortex; UF, uncinate fasciculus; VAP, ventral amygdalofugal pathway; VSP, ventral striatum pathway; see Figure 1 for abbreviations.
Coronal sections and photomicrographs from case M3 showing the distribution of anterograde label in the medial thalamus after bilateral BDA injections in the rSTG. Photomicrographs at 2 different magnifications illustrate the patchy distribution of the label in the magnocellular portion of the medial dorsal nucleus of the thalamus. Note the decreased density of label in the right hemisphere with the MTL ablation. Scale bar: 250 μm. Cln, central lateral thalamic nucleus; CnMD, centrum medianum thalamic nucleus; Cd, caudate nucleus; Pcn, paracentral nucleus; CeM, central medial thalamic nucleus; AD, anterior dorsal thalamic nucleus; AM, anterior medial thalamic nucleus; AV, anterior ventral thalamic nucleus; Cif, central inferior thalamic nucleus; Cim, central intermedial thalamic nucleus; MDmc, medial dorsal thalamic nucleus magnocellular division; MDmf; medial dorsal thalamic nucleus multiformis division; MDpc, medial dorsal thalamic nucleus parvocellular division; Pcn, paracentral nucleus; Pf, parafascicular nucleus; Re, Reuniens; Ro, Rotundus; sf, subfascicular nucleus.
(a,b) Photomicrographs from case M2 showing the disruption of the labeled fibers in the UF (UF,a–d), the VAP (e–h), and the VSP (i–n), after left MTL removal relative to the normal contralateral hemisphere. Scale barsa,b,e,f,i,j,m,n: 1 mm;c,d,g,h,k,l: 100 μm. ot, optic tract; ac, anterior commissure; H, Hippocampus.
(a,b) Photomicrographs from case M2 showing the disruption of the labeled fibers in the UF (UF,a–d), the VAP (e–h), and the VSP (i–n), after left MTL removal relative to the normal contralateral hemisphere. Scale barsa,b,e,f,i,j,m,n: 1 mm;c,d,g,h,k,l: 100 μm. ot, optic tract; ac, anterior commissure; H, Hippocampus.
Photomicrographs of the ventral medial frontal cortex comparing the label after rSTG injections in the normal and MTL-lesioned hemispheres of Case M2. Area inside dashed-outline rectangles in (a) and (e) shown at higher magnification in (b–d) and (f–h), respectively. Arrows identify labeled axons in photomicrographs at low and high power magnifications. Scale bar: 250 μm.
Lateral surface view and coronal sections (a–i) illustrating anterograde tracer injections in caudal STG (dark gray), with “opened” lateral sulcus shown in blue and resulting fiber and terminal label in case M4. Labeled fibers course through the white matter of the STG and the extreme and external capsules (i–f) rostrally and then just dorsal to the UF towards the frontal lobe. The pattern and density of label was the same in both hemispheres, suggesting that the MTL removal did not disrupt fibers from the caudal STG to the frontal lobe. A, amygdala; p, principal sulcus; see previous figures for abbreviations.
Summary diagrams of the major fiber pathways examined in this study. Left column of coronal sections illustrates projections from the rSTG to the frontal cortex and medial thalamus. The series of sections depicts each pathway's trajectory, from its origin in the injected cortical tissue (shown in black), to the course it follows through the white matter (black lines of varying thickness, representing graded size of projections), to its destination in cortex or thalamus (shown in shades of gray, representing graded density of terminal label). The projection from rSTG to the frontal cortex travels through the uncinate fasciculus (UF, +20). A major branch of this pathway continues medially to course below the striatum on the unoperated side (left hemisphere, solid line with arrowhead at +20) and then turns rostrally to terminate in medial and orbital frontal cortical areas on this side (left hemisphere, solid lines and dark gray shading at +24 and +30), with the highest density of terminal label in the ventral medial frontal cortical areas. Aspiration of the MTL (right MTL lesion at +7 through +20) transected this medial branch of the UF (right hemisphere, dashed line with arrowhead at +20) and, as a result, there was only sparse terminal label in the ventral medial frontal cortical areas on this side (right hemisphere, dashed lines with arrowheads and light gray shading at +24 and +30). Some fibers comprising the UF do not continue medially from their origin but, instead, turn dorsally and rostrally to travel through the external and extreme capsules (left hemisphere, solid lines at +15 and +20), after which they converge with the more medial branch of the uncinate fasciculis to terminate in mid and lateral orbital areas as well as in small frontal areas dorsally (left hemisphere, thin solid lines with arrowheads and light gray shading at +24 and +30). These branches of the UF escaped damage on the lesioned side and so the terminal label at their destinations was unaffected. The MTL removal also transected the caudally projecting fibers that join the VAP (at +15) and VSP (at +10 and +7), resulting in reduced terminal label in the medial thalamus (AN and MD at +10 and +7). Right column of coronal sections depicts projections to the frontal cortex from the injected areas of the auditory belt and parabelt divisions of the caudal STG. The MTL removal had no effect on these fiber pathways (solid black lines in all coronal sections, and so the terminal label was also unaffected (equivalent gray shading in both hemispheres at +24 and +30). AN, anterior thalamic nuclei; ai, arcuate sulcus, inferior; as, arcuate sulcus, superior; cc, corpus callosum; ci, cingulate sulcus; Cl, claustrum; Iag, insula, agranular subdivision; Idg, insula, dysgranular subdivision; los, lateral orbital sulcus; orl, lateral orbital sulcus; orm, medial orbital sulcus; FO, frontal operculum; fx, fornix; Gp, globus pallidus; H, hippocampus; Pu, putamen; sf, subfascicular nucleus; MD, medial dorsal thalamic nucleus; see Figure 1 for abbreviations.
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