Corticotectal Projections From the Premotor or Primary Motor Cortex After Cortical Lesion or Parkinsonian Symptoms in Adult Macaque Monkeys: A Pilot Tracing Study

Abstract

The corticotectal projections, together with the corticobulbar (corticoreticular) projections, work in parallel with the corticospinal tract (CST) to influence motoneurons in the spinal cord both directly and indirectly via the brainstem descending pathways. The tectospinal tract (TST) originates in the deep layers of the superior colliculus. In the present study, we analyzed the corticotectal projections from two motor cortical areas, namely the premotor cortex (PM) and the primary motor cortex (M1) in eight macaque monkeys subjected to either a cortical lesion of the hand area in M1 (n = 4) or Parkinson's disease-like symptoms PD (n = 4). A subgroup of monkeys with cortical lesion was subjected to anti-Nogo-A antibody treatment whereas all PD monkeys were transplanted with Autologous Neural Cell Ecosystems (ANCEs). The anterograde tracer BDA was used to label the axonal boutons both en passant and terminaux in the ipsilateral superior colliculus. Individual axonal boutons were charted in the different layers of the superior colliculus. In intact animals, we previously observed that corticotectal projections were denser when originating from PM than from M1. In the present M1 lesioned monkeys, as compared to intact ones the corticotectal projection originating from PM was decreased when treated with anti-Nogo-A antibody but not in untreated monkeys. In PD-like symptoms' monkeys, on the other hand, there was no consistent change affecting the corticotectal projection as compared to intact monkeys. The present pilot study overall suggests that the corticotectal projection is less affected by M1 lesion or PD symptoms than the corticoreticular projection previously reported in the same animals.

Keywords: Parkinson; anterograde tracing; brainstem; cortical lesion; motor cortex; non-human primate; spinal cord injury.

Figure 1

Typical distribution of BDA labeled corticotectal axonal boutons in the ipsilateral superior colliculus (SC) in two representative monkeys subjected to unilateral primary motor cortex (M1) lesion (A). In both monkeys, BDA was injected in the ipsilesional premotor cortex (PM). In panel (A), Mk-VA was treated with an anti-Nogo-A antibody whereas in Mk-BI was untreated (B). Only the ipsilesional SC is shown. Axonal boutons are depicted with green dots. The histological sections are arranged from rostral to caudal. The (C) illustrates a typical BDA labeled terminal field in the SC, with axon segments as well as a few boutons pointed by arrows. See list of abbreviations.

Figure 2

Same as in Figure 1, but for two representative Parkinson’s disease (PD) monkeys. Note that one monkey (Mk-MY, A) was injected with BDA in PM, whereas the injection was in M1 in the second monkey (Mk-LY, B).

Figure 3

Scatter plots of the total numbers of corticotectal boutons observed in the SC in the different groups of monkeys subjected to motor cortex injury (MCI) or MPTP intoxication (PD). The data are restricted to the ipsilateral SC with respect to the BDA injection site, either in PM or M1. For comparison, the corresponding data in intact monkeys (Fregosi and Rouiller, 2017) are represented here by the range derived from intact cases (yellow or light blue areas), with individual data points in blue (PM projection in intact monkeys) or in brown (M1 projection in intact monkeys). The individual data points for the corticotectal projections (present study) are indicated with black or open white symbols for absolute data or normalized data, respectively (A,B, respectively). The BDA injection site (PM or M1) is indicated below the graph. Panel (A) is for the absolute numbers of corticotectal boutons, whereas (B) is for normalized numbers of corticotectal boutons. The presence/absence of treatment is indicated below the graphs. In both panels, the data were corrected with respect to the distance between consecutive sections (see “Materials and Methods” section). For Mk-RO, the vertical arrow indicates that the number of axonal boutons in SC was underestimated, due to a few missing histological sections (see “Results” section).

Figure 4

Distributions of the numbers of BDA-labeled corticotectal axonal boutons both en passant and terminaux in the ipsilateral SC, across the different SC layers in each monkey (see “List of Abbreviations”), subjected to cortical lesion of the hand area in M1 motor cortex injury (MCI, A), or to MPTP intoxication (PD, B,C). In (A), the top two monkeys were treated with the anti-Nogo-A antibody, whereas the bottom two monkeys were untreated. In panels (B,C), all monkeys were autologous neural cell ecosystems (ANCEs) treated. In each graph, the sum of all bins is 100%.