Elephant facial motor control

Abstract

We studied facial motor control in elephants, animals with muscular dexterous trunks. Facial nucleus neurons (~54,000 in Asian elephants, ~63,000 in African elephants) outnumbered those of other land-living mammals. The large-eared African elephants had more medial facial subnucleus neurons than Asian elephants, reflecting a numerically more extensive ear-motor control. Elephant dorsal and lateral facial subnuclei were unusual in elongation, neuron numerosity, and a proximal-to-distal neuron size increase. We suggest that this subnucleus organization is related to trunk representation, with the huge distal neurons innervating the trunk tip with long axons. African elephants pinch objects with two trunk tip fingers, whereas Asian elephants grasp/wrap objects with larger parts of their trunk. Finger "motor foveae" and a positional bias of neurons toward the trunk tip representation in African elephant facial nuclei reflect their motor strategy. Thus, elephant brains reveal neural adaptations to facial morphology, body size, and dexterity.

Fig. 1.. Extraordinary size and neuron number of the elephant facial nucleus.

(A) Micrograph of a coronal Nissl-stained 60-μm brainstem section of the adult Asian elephant cow Burma. The section stems from midlevel of the facial nucleus (white outline). D, dorsal; L, lateral. (B) Somata drawing and facial nucleus outline. (C) Micrograph [dashed area in (B)]. (D) Top: Facial subnuclei of the section in (B) highlighted in color. Bottom: Color-coded musclelotopy suggestion. (E) Somata drawings of facial nuclei of various mammals, scale as (B). (F) Facial nucleus neuron number in mammals. Species averages are given in black [dots data (5); triangles data (6)]. In red, data are given for individual African and Asian elephant facial nuclei; filled symbols (cell counts), empty symbols (facial nerve fiber counts), squares (stillborn elephants), dots (adult elephants) (see fig. S1). Photo credit (D): Michael Brecht, Humboldt-Universität zu Berlin; Zoologischer Garten Berlin, Berlin, Germany.

Fig. 2.. Allometry of brain weight and facial nucleus neuron number in mammals.

Facial nucleus neuron number (y axis) versus brain weight (x axis). All data points are species averages; data as specified in Fig. 1F. Blue dashed line, power function (exponent 0.2988) fitted to the data of all mammals. Black line power function (exponent 0.1641) fitted to the data of primates. Both dolphins and elephants have many more facial neurons than predicted by the power function for primates.

Fig. 3.. Asian and African elephant ears, ear (auricularis) motor innervation, and the medial facial subnuclei.

(A) Ears of Asian (left) and African (right) elephants differ. (B) Auricularis and main branch of the facial nerve of an Asian (left) and African (right) baby elephant. The auricularis branch (innervating the ear) is thicker in the African elephant. (C) Drawings of left facial nucleus and somata of an Asian elephant (left) and an African elephant (right). Medial subnucleus cells are highlighted in red. Sections are taken at the maximal extent of medial subnuclei. The medial subnucleus innervates ear muscles in mammals. (D) Absolute neuron (circles) and axon (squares) number (left) and percentage (of total facial nucleus neurons, right) of medial subnucleus in Asian (empty symbols) and African (solid symbols) elephant facial nuclei. P values refer to unpaired t tests of cell counts only and would be lower if fiber counts were included. Photo credit (A and B): Lena V. Kaufmann, Humboldt-Universität zu Berlin; (A, left) Zoologischer Garten Berlin, Berlin, Germany; (A, right) Zoo Schönbrunn, Vienna, Austria.

Fig. 4.. Cell size gradients and extremely large neurons in the dorsal subnucleus of the elephant facial nucleus might be related to trunk innervation.

(A) Trunk of African elephant cow Aruba. (B) Somata drawing of a coronal Nissl-stained 60-μm section through the left facial nucleus of Aruba (dorsal subnucleus outlined). (C) Drawing of the elongated dorsal subnucleus with its soma size gradient. (D) Top: Proximal neuron micrograph. Bottom: Large distal neuron micrograph (soma diameter, 104 μm). (E) Left: Plot of estimated soma volume in the dorsal subnucleus as shown in (B) and (C) against subnucleus position. The correlation is significant (P < 0.05). Right: Plot of estimated axon volume for trunk innervating facial nucleus neurons. See fig. S2. Photo credit (A): Petra Prager.

Fig. 5.. Cell size gradients in the dorsal facial subnucleus of the elephants are not seen in dorsolateral facial subnuclei of other mammals.

(A) Left: Somata drawing of a coronal Nissl-stained 60-μm section through the left facial nucleus of African elephant cow Aruba (dorsal subnucleus outlined). Right: Plot of soma area (normalized to average soma size in the subnucleus) in the dorsal subnucleus against cell position in the dorsal subnucleus. Cell position is plotted in percentage of the longitudinal axis of the subnucleus; the counting direction and orientation of the longitudinal axis is indicated by the arrow (left). A linear regression line is superimposed (black); the correlation was significant [Spearman’s Rho; P (two-tailed) = 0.0]. (B) Left: Same as (A) but for the Asian elephant cow Burma. Right: Same as (A) but for the Asian elephant cow Burma. [Spearman’s Rho; P (two-tailed) = 0.0]. (C to F) Same analysis as in (A) and (B) but for the dorsolateral facial subnucleus of various mammals, which typically represents nose/anterior rostrum muscles. The data stem from the online accessible BrainMaps database. (C) Left: Same as (A) but for the macaque monkey; cells in the dorsolateral nucleus are shown in black; other facial nucleus cells are shown in gray [Spearman’s Rho; P (two-tailed) = 0.046]. (D) Same as (C) but for the cat. A linear regression line is superimposed (dashed); the correlation was not significant [Spearman’s Rho; P (two-tailed) = 0.28]. (E) Same as (D) but for the mouse [Spearman’s Rho; P (two-tailed) = 0.20]. (F) Same as (D) but for the short-tailed opossum [Spearman’s Rho; P (two-tailed) = 0.65].

Fig. 6.. Asian-African elephant differences in putative trunk finger motor foveae and motor strategies.

(A) African elephants tend to pinch objects with their two fingers (15), thus engaging the trunk tip. (B) African elephant trunks have two fingers, a dorsal (DF) and ventral (VF) one. (C) Overlay of somata from five coronal 60-μm sections from around the anterior third of the facial nucleus of African elephant Aruba. DF? and VF? denote the putative dorsal and ventral finger representation. Note the high cell density motor foveae and the shape similarity to (B). (D) Asian elephants tend to grasp/wrap objects with their trunk (15), thus engaging larger trunk parts. (E) Asian elephant trunks have one dorsal finger (DF). (F) Somata overlay from the Asian elephant Burma, conventions as in (C). High cell density foveae are less evident than in (C). (G) Neurons are preferentially distributed distally (toward the putative trunk tip) in the dorsal subnucleus of African elephants compared to Asian elephants. Bottom: Somata overlay of dorsal subnucleus from African elephant Aruba (C) and Asian elephant Burma (F) arranged horizontally (distal to the right). Note the rightward/distal cell bias in the African elephant. Top: Cell distribution along the proximal-distal axis of dorsal subnuclei in six African (solid line) and six Asian (dashed line) elephant facial nuclei. Cell numbers were similar proximally but very different distally (t tests, *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001). (H) Distal distribution bias in the lateral subnucleus (toward the putative tip representation) in African elephants. Conventions as in (G). Photo credit (A), (B), and (E): Lena V. Kaufmann, Humboldt-Universität zu Berlin; (A) Zoo Schönbrunn, Vienna, Austria. Photo credit (D): Michael Brecht, Humboldt-Universität zu Berlin; Zoologischer Garten Berlin, Berlin, Germany.