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. 2012 Aug;22(8):1834-50.
doi: 10.1093/cercor/bhr257. Epub 2011 Sep 27.

Topographic Maps within Brodmann's Area 5 of macaque monkeys

Adele M H Seelke  1 , Jeffrey J Padberg, Elizabeth Disbrow, Shawn M Purnell, Gregg Recanzone, Leah Krubitzer
Affiliations

Topographic Maps within Brodmann's Area 5 of macaque monkeys

Adele M H Seelke et al. Cereb Cortex. 2012 Aug.

Abstract

Brodmann's area 5 has traditionally included the rostral bank of the intraparietal sulcus (IPS) as well as posterior portions of the postcentral gyrus and medial wall. However, different portions of this large architectonic zone may serve different functions related to reaching and grasping behaviors. The current study used multiunit recording techniques in anesthetized macaque monkeys to survey a large extent of the rostral bank of the IPS so that hundreds of recording sites could be used to determine the functional subdivisions and topographic organization of cortical areas in this region. We identified a lateral area on the rostral IPS that we term area 5L. Area 5L contains neurons with receptive fields on mostly the shoulder, forelimb, and digits, with no apparent representation of other body parts. Thus, there is a large magnification of the forelimb. Receptive fields for neurons in this region often contain multiple joints of the forelimb or multiple digits, which results in imprecise topography or fractures in map organization. Our results provide the first overall topographic map of area 5L obtained in individual macaque monkeys and suggest that this region is distinct from more medial portions of the IPS.

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Figures

Figure 1.
Figure 1.
Architectonic parcellation of the IPS by different studies. The first scheme was proposed by Brodmann (A) and subsequent schemes with differing terminology were proposed by different investigators (B–D). In some modern parcellation schemes, BA5 has been subdivided into at least 2 fields. For abbreviations, see Table 1.
Figure 2.
Figure 2.
The location of recording sites in different portions of BA5 in different studies. Some studies were in a middle portion of BA5 (A–C,G,I), some studies recorded from medial portion of BA5 (D–F,H), and some studies recorded from lateral portion of area 5 (E,G,J,K). These recording sites do not always correspond to architectonic subdivisions within BA5. The arrows indicate anatomic directions, and the scale bar is for D–K. Conventions as in previous figure.
Figure 3.
Figure 3.
A dorsolateral drawing of the brain (A) showing the locations from which sections B–D were taken (gray bars). (B) High-powered images of cortex sectioned horizontally and stained for Nissl allow for a direct comparison of the laminar organization of areas 2, area 5L, and the presumptive area MIP. (C) The area 2 and presumptive MIP border are characterized by a dramatic decrease in cell density of layers IV and VI in MIP? as well as a thickening of these layers. (D) The area 2/5L boundary is characterized by a slight decrease in density and a thickening of layers IV and VI. These differences are not as distinct as those between the borders of area 2 and MIP?. In the flattened preparations that have been stained for myelin (E and F) some of the borders of areas 5L and MIP are visible. However, the entire series of sections is used to determine all of the boundaries of these fields. This type of preparation allows much of the length of individual recording tracks within the IPS to be readily appreciated (black arrows). Cortical field boundaries are marked by an arrow in C and D and with a dashed line in E and F. Photomicrographs were taken from cases 01-45 (F); 03-141 (D); 04-51 (B: area 2); 04-53 (B: MIP? and C); 05-82 (E); 05-116 (B: area 5L). Conventions as in previous figures.
Figure 4.
Figure 4.
Histograms depicting the percentage of recording sites in which neurons in anterior and posterior parietal areas responded to (A) cutaneous versus deep stimulation or (B) visual, bilateral, or ipsilateral stimulation. The submodality to which neurons respond is distinct across cortical areas. The responsiveness of neurons to visual stimulation in area MIP is one of the distinguishing features of this field. Mean + standard deviation, P < 0.05. *—significantly different from cutaneous. †—significantly different from all other areas.
Figure 5.
Figure 5.
Maps of area 5L and portions of area 2 generated from electrophysiological recordings in the 3 cases (A. 05-82, B. 03-141, and C. 04-51). In these cases, most of the neurons in area 5 were responsive to stimulation of deep receptors of the skin, muscle, and joints (closed circles). In 2 cases, there were a few sites in which neurons responded to visual stimulation (A and B; gray circles) and in 2 cases, neurons had bilateral receptive fields (A and B; gray squares). The topographic organization of area 2 could be readily discerned, but in area 5L, the same body part was represented multiple times and was encompassed in different receptive field configurations. Furthermore, only the forelimb, and not the head or trunk, was represented in area 5L. Also, there was a greater degree of variability in map organization between individual cases in area 5L compared with area 2. The representations of digits 1 (blue) and 2 (yellow) are highlighted so that direct comparisons can be made between areas 2 and 5L. Area 2 has distinct individual representation of both D1 and D2 while this is variable in area 5L. Most often these digits are represented with other digits rather than individually in area 5L. Thick solid and dashed lines indicate architectonic borders and thin lines separate different body part representation with each cortical area. The red outlines area 5L. The IPS is denoted as a thick black line that runs through area 5L in the mediolateral plane. Other conventions as in previous figures.
Figure 6.
Figure 6.
Maps of area 5L and portions of area 2 generated from densely spaced electrophysiological recordings in 3 monkeys (A. 07-64, B. 03-117, and C. 05-116). In these cases, about half of the neurons in area 5L were responsive to stimulation of deep receptors of the skin, muscle, and joints (closed circles) and about half of the sites were unresponsive to any type of stimulation (black X). In one case, there were a few sites in which neurons responded to visual stimulation and 4 sites in which neurons had bilateral receptive fields (C). The topographic organization of area 2 could be readily discerned, but in area 5, the same body part was represented multiple times and was included in many different receptive field configurations. Furthermore, only the forelimb was represented in area 5L. Conventions as in previous figures.
Figure 7.
Figure 7.
Examples of receptive field composition for neurons in area 5L from 4 cases (A–D). These examples demonstrate that receptive fields were complex and often involved several different portions of the forelimb such as the knuckles, wrist, and elbow (A) or elbow and shoulder (B; bottom figure). In some cases, neurons had bilateral receptive fields (B; top figure). Multiple digits were often encompassed in a receptive field (C) or relatively large portions of the palm were represented (D). Neurons at all of these sites responded to manipulation of the joints and muscles or taps to portions of the skin. The small insets below each case number illustrate portions of area 2 and area 5L and the location of the recording sites within area 5L that correspond to the receptive fields drawn for each case.
Figure 8.
Figure 8.
A map of the medial half of the rostral bank of the IPS (A) and the location of the recording sites relative to the CS and IPS. Unlike area 5L, this medial IPS region contains numerous sites where neurons are responsive to visual stimulation and more sites in which receptive fields were ipsilateral or bilateral. (B) Examination of receptive field progression demonstrates that as recording sites move from medial to lateral (sites 1–5 in A), corresponding receptive fields progress from hindlimb, trunk, to forelimb. Thus, the entire body appears to be represented in the medial region. However, like area 5L, the same body part can be represented multiple times in different locations. Conventions as in previous figures.
Figure 9.
Figure 9.
A summary of the functional subdivisions of anterior parietal areas 3a, 3b, 1, and 2 and posterior parietal areas 5L and the presumptive MIP. While anterior parietal areas have a clear parallel mediolateral organization, this type of organization is not observed in posterior parietal areas. Both MIP? and area 5L have fractured maps that are dominated by representations of the digits, hand, and forelimb. The solid gray corresponds to BA5 and area 5L and the presumptive MIP depicted here fall within this larger zone. Noted that in areas 3b and 1, all digits are represented individually, while in areas 3a and 2, only digits 1 and 2 are represented individually; digits 3–5 are generally represented together. In area 5L, sometimes digit 1 or 2 is represented individually, but most often multiple digits are represented in different combinations (light blue stipple) or parts of the hand or the whole hand is represented (light purple). General topographic organization of areas 3a, 3b, 1, and 2 are redrawn from data from the current study and that of Krubitzer et al. (2004), Nelson et al. (1980), and Pons et al. (1985b), respectively; the genital/tail representation in areas 3b and 1 is from Rothemund et al. (2002). Conventions as in previous figures.
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