Differential Impact of Parvocellular and Magnocellular Pathways on Visual Impairment in Apperceptive...

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This article was downloaded by: [Dalhousie University] On: 03 October 2014, At: 00:28 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Neurocase: The Neural Basis of Cognition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/nncs20 Differential Impact of Parvocellular and Magnocellular Pathways on Visual Impairment in Apperceptive Agnosia? Helmut Hildebrandt a b , Cathleen Schütze a c , Markus Ebke a & Karoline Spang c a Municipal Hospital of Bremen , Neurology , Bremen, Germany b Institute for Psychology, University of Oldenburg , Oldenburg, Germany c Institute for Human-Neurobiology, University of Bremen , Bremen, Germany Published online: 02 Feb 2010. To cite this article: Helmut Hildebrandt , Cathleen Schütze , Markus Ebke & Karoline Spang (2004) Differential Impact of Parvocellular and Magnocellular Pathways on Visual Impairment in Apperceptive Agnosia?, Neurocase: The Neural Basis of Cognition, 10:3, 207-214, DOI: 10.1080/13554790490495168 To link to this article: http://dx.doi.org/10.1080/13554790490495168 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions

Transcript of Differential Impact of Parvocellular and Magnocellular Pathways on Visual Impairment in Apperceptive...

Page 1: Differential Impact of Parvocellular and Magnocellular Pathways on Visual Impairment in Apperceptive Agnosia?

This article was downloaded by: [Dalhousie University]On: 03 October 2014, At: 00:28Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Neurocase: The Neural Basis of CognitionPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/nncs20

Differential Impact of Parvocellular and MagnocellularPathways on Visual Impairment in ApperceptiveAgnosia?Helmut Hildebrandt a b , Cathleen Schütze a c , Markus Ebke a & Karoline Spang ca Municipal Hospital of Bremen , Neurology , Bremen, Germanyb Institute for Psychology, University of Oldenburg , Oldenburg, Germanyc Institute for Human-Neurobiology, University of Bremen , Bremen, GermanyPublished online: 02 Feb 2010.

To cite this article: Helmut Hildebrandt , Cathleen Schütze , Markus Ebke & Karoline Spang (2004) Differential Impact ofParvocellular and Magnocellular Pathways on Visual Impairment in Apperceptive Agnosia?, Neurocase: The Neural Basis ofCognition, 10:3, 207-214, DOI: 10.1080/13554790490495168

To link to this article: http://dx.doi.org/10.1080/13554790490495168

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of theContent. Any opinions and views expressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information. Taylor and Francis shall not be liable forany losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveror howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use ofthe Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Page 2: Differential Impact of Parvocellular and Magnocellular Pathways on Visual Impairment in Apperceptive Agnosia?

Differential Impact of Parvocellularand Magnocellular Pathways on VisualImpairment in Apperceptive Agnosia?

Helmut Hildebrandt1,2, Cathleen Schutze1,3, Markus Ebke1 and Karoline Spang3

1Municipal Hospital of Bremen, Neurology, Bremen, Germany, 2Institute for Psychology, University of Oldenburg,Oldenburg, Germany and 3Institute for Human-Neurobiology, University of Bremen, Bremen, Germany

Abstract

The term ‘‘visual form agnosia’’ describes a disorder characterized by problems recognizing objects, poor copying,and distinguishing between simple geometric shapes despite normal intellectual abilities. Visual agnosia hasbeen interpreted as a disorder of the magnocellular visual system, caused by an inability to separate figure from groundby sampling information from extended regions of space and to integrate it with fine-grain local information. However,this interpretation has hardly been tested with neuropsychological or functional brain imaging methods, mainlybecause the magnocellular and parvocellular structures are highly interconnected in the visual system.

We studied a patient (AM) who had suffered a sudden heart arrest, causing hypoxic brain damage. Hewas/is severely agnosic, as apparent in both the Birmingham Object Recognition Battery and the Visual Object andSpace Battery. First- and especially second-order motion perception was also impaired, but AM experiencedno problems in grasping and navigating through space. The patient revealed a normal P100 in visualevoked potentials both with colored and fine-grained achromatic checkerboards. But the amplitude of the P100 wasclearly decreased if a coarse achromatic checkerboard was presented.

The physiological and neuropsychological findings indicate that AM experienced problems integratinginformation over extended regions of space and in detecting second-order motion. This may be interpreted as adisorder of the magnocellular system, with intact parvocellular system and therefore preserved ability to detect bothlocal features and colors.

Introduction

Benson and Greenberg (1969) described a syndrome which

they named ‘‘visual form agnosia.’’ The case they described

suffered from no serious intellectual impairment, but from

object recognition problems and poor copying abilities. As

shown by Efron (1969) the patient was unable to distinguish

between simple geometric shapes. Several other patients

with similar impairments have been described (Adler,

1944, 1950; Abadi et al., 1981; Campion and Latto, 1985).Extensive testing of these patients showed multiple dissocia-

tions between ‘‘figure-ground separation’’ (Kartsounis and

Warrington, 1991), ‘‘shape discrimination (Davidoff and

Warrington, 1993), and ‘‘luminance and color discrimina-

tion’’ (Heywood et al., 1994). These dissociations have been

taken as an argument for segregated visual pathways in the

human brain, which can be lesioned focally and therefore

produce different classes of symptoms. A subgroup of these

patients cannot distinguish between different shapes, sizes,

and shadings of grey. One popular explanation for these

symptoms proposes a selective damage of the magnocellular

visual pathway (Milner et al., 1991; Davidoff and Warrington,

1993).

The term ‘‘magnocellular’’ refers to a subdivision of the

visual system originating in the alpha ganglion cells of theretina, projecting to layers 4B and 4C of the striate cortex

(V1), and thence to the ‘‘thick stripes’’ of the adjacent area

V2 (Livingstone and Hubel, 1988). The magnocellular path-

way is supposed to predominantly analyse depth and motion

cues, while it is ‘‘color blind.’’ On the other hand, because of

the larger receptive fields of its neurons, it has also been

related to the perception of size and length differences

Neurocase2004, Vol. 10, No. 3, pp. 207–214

Correspondence to: Helmut Hildebrandt, University of Oldenburg, Institute of Psychology, 2611 Oldenburg, Germany. e-mail: [email protected]

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(Kosslyn et al., 1989, 1990), to perception of low spatial

frequencies (i.e., coarse spatial information) and therefore of

surfaces or entities in figure-ground separation (Milner et al.,

1991).

Though many of the problems of patients suffering from

visual form agnosia can be explained by an isolated lesion

of the magnocellular system, not all form agnosic patients

have problems in recognizing motion and in localizingobjects for action. Based on the importance of the magno-

cellular pathway for motion processing, one would predict

that any lesion of this system should severely impair motion

perception (for an extended discussion of this aspect, see

Goodale and Milner, 1995). Motion perception was tested

extensively only in the case of Milner et al. (1991), D.F.

and her motion perception was indeed impaired. Neither

Bartolomeo et al. (1998) nor Davidoff and Warrington(1993), Ferreira et al. (1998) or Kartsounis and Warrington

(1991) reported an impairment of motion perception in their

cases.

One possibility to reconcile these apparently contradictory

findings is that motion perception has not been investigated

extensively in visual form agnosic patients because the

impairment was so subtle that it did not produce obvious

clinical deficits. For example, only higher-order motion de-tection may be affected while first-order motion detection,

relying on luminance changes, remains intact (Chubb and

Sperling, 1988; Cavanagh and Mather, 1989; Smith et al.,

1994; Braun et al., 1998).

Another possibility is to postulate different magnocellular

subsystems of visual information processing responsible for

low spatial frequencies, for motion perception and for object

localization. Low and high spatial frequencies are indeedprocessed predominantly in different parts of the brain (Fink

et al., 1997, 1999) and may be disturbed differentially after

brain lesions (Robertson and Lamb, 1991), although the

hemispheric difference in global/local processing only be-

comes apparent at later stages of information processing

(Heinze et al., 1998). A strong argument for such a separation

of the magnocellular pathway comes from reading research.

Patients with developmental dyslexia show poor control ofsaccades (Biscaldi et al., 1994, 1998) and impaired visual-

spatial attention (Facoetti et al., 2000). They show differences

in the structure of their magnocellular neurons at the lateral

geniculate nucleus (Livingstone et al., 1991) and in the

physiological activity of magno-recipient areas such as MT

(Eden et al., 1996; Sperling et al., 2003; Stein, 2003). But

clearly dyslexic patients are not as impaired in motion per-

ception and grasping (visuomotor integration) as they are inreading.

Patients with visual form agnosia were also impaired in

reading (Kartsounis and Warrington, 1991; Milner et al.,

1991; Davidoff and Warrington, 1993; Bartolomeo et al.,

1998; Ferreira et al., 1998), but not necessarily in shape

perception (Kartsounis and Warrington, 1991), and in identi-

fying single letters. Recent investigations have shown that in

normal readers the separation of the letters in letter strings

involves primarily the magnocellular pathway, whereas single

letter reading depends on parvocellular activity (Omtzigt

et al., 2002). The high incidence of reading impairments in

visual form agnosia may therefore support the explanation

of their deficits in terms of damage to the magnocellular

pathway.

Visual evoked potentials (VEPs) provide useful neuro-

physiological information with respect to the functioning ofthe two systems. Two predictions can be made in this

respect: (1) Selective damage of the magnocellular pathway,

leaving the parvocellular pathway intact, should result in an

intact P100 when using a checkerboard defined by color,

independent of the square size since the parvocellular-blob

pathway processes color-defined stimuli for all visible spa-

tial frequencies (Tobimatsu et al., 1995; Spinelli et al., 1996;

Arakawa et al., 1999). (2) If the magnocellular systeminvolves the sampling of low spatial frequencies, then

achromatic checkerboards consisting of small squares should

produce a normal VEP whereas a checkerboard with rela-

tively large squares should evoke clearly smaller VEP ampli-

tudes (Livingstone et al., 1991). In particular, the amplitude

of the N1/P1 complex reflects spatial frequency (Tobimatsu

et al., 1995; Arakawa et al., 1999). In achromatic checker-

boards this amplitude increases only with patterns of aspatial frequency well above 2 cycles per degree, whereas

in chromatic checkerboards it decreases starting at 2 cycles

per degree.

Recently, we studied a patient with visual form agnosia

due to sudden heart arrest using a series of neuropsycho-

logical tests and investigating first and second order motion

perception. Moreover cortical sum potentials were evoked

by reversing achromatic and colored checkerboards ofdifferent sizes.

Case description

AM, a technical drawer, suffered from sudden heart arrest

when he was 46 years-old. He was reanimated and awoke

from coma three days after the incident. Five weeks after

his acute medical treatment, AM was admitted to a neu-rological rehabilitation unit where all the investigations

reported below took place. At this time, he had no obvious

motor problems, was aware of having visual and memory

problems, but was disoriented in time and place. No

confusional state was evident, although he left the hospital

several times without being allowed to do so. His mood

state alternated between calm and anxious, but he never

became really upset or aggressive. The patient was alwaysmotivated to participate in the investigations and in train-

ing sessions, and became tired only after one hour of

testing.

A neurological examination showed intact motor, sensori-

motor and cranial nerve functions. There was no visual field

defect as tested with a Goldman Perimeter. A 1.5 Tesla MRI

scan, taken 2 months after the heart arrest, showed no focal

damage and no major brain atrophy.

208 H. Hildebrandt et al.

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Neuropsychological investigation

Visual fields during visual extinction

We used the TAP-Neglect test (see Hildebrandt et al., 2002,

for an extensive description) to analyze the visual fields of

AM during visual extinction. The test was performed in a

dimmed room, with maximal screen contrast and a 21-inch

screen. AM had no visual field deficits, but response timesespecially to targets on the left side were increased (725 ms for

left-sided targets and 602 ms for right-sided targets), and he

also missed one item there.

Clinical testing of visual perception

Illusionary contoursA set of high frequency gratings were shown to AM and hehad to decide whether or not a simple geometric figure was

hidden in these gratings, defined by small line breaks. AM had

no problems identifying circles and squares in the gratings,

although his reactions were slow and he gave the impression

of not always feeling totally sure.

Kanisza figuresA set of Kanisza figures was presented and AM’s task was torecognize the figures. To enhance the sensitivity to impair-

ment we started with distorted figures (rotating one or two of

the Pac-men by about 90 degrees and then gradually back

rotating these circles). AM was able to discriminate between

the conditions, although his reactions were again slow and

appeared sometimes uncertain.

Color perceptionA set of colored squares was shown on a computer monitor

and AM was asked to name the colors. This turned out to be a

very easy task for him.

Copying and visuoconstructional abilitiesWhen copying the complex Rey-Osterrieth figure, AM started

in a piecemeal fashion and ended up with just a partial

solution, documenting some visuoconstructional problems(see Fig. 1).

In the Gailinger Abzeichentest (Gailinger copy test) geo-

metrical figures have to be copied on a sheet of paper with

dots, indicating specific parts of the original figure. Some of

these figures require three-dimensional perception. AM had

no major problems perceiving the three-dimensional figures

but in assessing the relative length of parts of the figures, and

made four errors during copying (see Fig. 2).In the Block Design test of the WAIS AM’s score was 5,

indicating a medium impairment.

ReadingAM could read single letters if the letters were spatially

separated (independent of font type). The ability to read

words depended on two aspects: First, he performed much

better in reading fonts like ‘‘Arial’’ than ‘‘Times Roman,’’

probably because the letters in ‘‘Arial’’ lack serifs. Second, his

reading ability depended on letter size: words written in small

letters (letter size < 16 pt.) led to confusions between letters.

Neuropsychological testing of visualabilities of AM

Space perception was investigated with the Visual Object

and Space Perception Battery (VOSP, see Table 1) and the

Birmingham Object Recognition Test (BORB, see Table 2).

Because the control data used in BORB reflect a 65þ age

group, we additionally collected data from 11 control subjects

(mean age of 49 years, minimum age of 43, maximum age of

54 years). AM scored in all spatial tasks BORB below therange of our control group, but in the normal range of the

Fig. 1. Copy of the Rey-Osterrieth Figure. Notice the piecemeal fashion of thecopy.

Fig. 2. Item of the Gailinger Abzeichentest.

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original BORB control group for two tasks: the ‘‘orientation

match task’’ and the ‘‘position of gap task,’’ both requiring acomparison of directions. Furthermore, AM’s performance

was normal in the screening task and in dot counting of the

VOSP.

Identifying nonoverlapping figures, examined with the

subtest of the BORB, was possible for single letters (AM

misnamed 2 of 18 letters, but this may be due to his first

language being Iranian) and almost perfect for geometrical

shapes (3 misidentifications on 36 trials). Identification ofsingle line drawings (14 errors in 40 trials), of paired letters

and of triplets was impaired (13 errors on 36 presentations of

paired letters and 28 errors out of 36 presented triplets). The

same held for triplets of shapes (10 mistakes on 36 trials) but

less so for paired geometrical shapes (2 errors on 36 trials).

Overlapping letters, geometrical shapes and line drawings

could hardly be identified. In general, AM replied correctly on

less than half of the trials with the exception of geometricalshapes, on which he performed slightly better (he misidenti-

fied only 8 out of 36 paired stimuli presented and 22 out of 54

triplets presented). However, this performance is far below thenormal range.

Object recognition was also investigated with the VOSP

and BORB (see Tables 1 and 2). AM scored in all of these

tasks below the range of our control group. He was also

impaired on all these tasks taking the results of the original

BORB control group, except for ‘‘association match’’ and

partly for ‘‘picture naming’’ of the BORB. In the case of

picture naming his identification of animals was in the normalrange, whereas the naming of manmade objects was highly

impaired. His errors in the association match task involved

only manmade objects, but not animals. It is worth noticing

that the only four correct answers AM gave in the Silhouette

task of the VOSP all concerned animals. We further tested this

difference by means of pictures of the Rivermead Behavioural

Memory Test using 16 animals and 16 manmade objects.

AM identified all 16 animals correctly, but only 13 of themanmade objects.

Table 1. Results in the visual object and space perception battery

Visual space perception Object recognition

VOSP Correct trials Cut-off score Correct trials Cut-off score

Shape detection (screening task) 18 �15 Incomplete letters 8 �17Dot numerosity 10 �8 Foreshortened Silhouettes 4 (only animal pictures) �16Visual location 13 �18 Object recognition 2 �15Spatial location 3 �7

Performance in tests written in italics was impaired.

Table 2. Results in the Birmingham object recognition battery

Visual space perception Object recognition

BORB Correct trials(maximum)

Controlsa

Mean (SD)Range of controlsa

& (cut-off scoreBORBb)

Correct trials(maximum)

Controlsa

Mean (SD)Range of controlsa

& (cut-off scoreBORBb)

Length matchtask

18 (30) 26.6 (1.6) 24–30 (<24) Minimal featurematch

16 (25) 24.8 (0.4) 24–25 (< 19)

Size match task 22 (30) 27.7 (2.3) 24–30 (<25) Foreshortenedmatch

15 (25) 24.5 (0.5) 24–25 (< 16)

Orientationmatch task

20 (30) 25.3 (1.4) 23–28 (<20) Object decision(easy)

22 (32) 31.7 (0.6) 30–32 (< 28)

Position of gapmatch task

28 (40) 34.8 (2.4) 30–39 (<27) Item match 25 (32) 32 (0) 32–32 (< 26)

Association match 25 (30) 29.6 (0.8) 28–30 (< 22)Picture naming

(short version)Animate drawings

10 (15) 14.4 (0.8) 13–15 (< 8)

Picture naming ofinanimatedrawings fromSubtest 7

12 (20) 20 (0) 20–20 (< 17)

Picture naming(long version)

50 (76) 73.8 (2.4) 69–76 (< 64)

aEleven age-matched control subjects were tested with the BORB.bScores of the BORB control group.Performance in tests written in italics was below the cut-off scores of the BORB. But note that AM scored outside the range of our control group in all subtests.

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Motion perception

First-order and second-order motion perception was inves-

tigated using sets of moving random dots (Braun et al.,1998). For each kind of motion the subject had to identify

the direction of motion of a small rectangle, at 108 distance

on the right or on the left of a central fixation point, moving

upwards or downwards on the screen. The target was defined

as a rectangle area with dots moving preferentially in one

direction, while dots in the remainder of the screen moved in

random directions. The coherence of the dots in the target

was varied between 0% (random, no coherence) and 100%(all dots in one direction, perfect coherence), and the mini-

mal amount of coherence required by the patient to identify

the motion direction of the target was measured. In the first

type of motion condition, the dots within the target area

moved coherently in the same direction as the target itself

(¼ first-order motion). In the second condition, the dots

within the rectangle were moving in the opposite direction

as the target itself (¼ second-order motion). In this condi-tion, the elementary movement detectors signal the direction

of the dots, not that of the target (cf. Braun et al., 1998),

and thus higher-order detectors are required to give correct

responses to upward or downward motion of the target

(Theta-motion).

Stimuli were produced by a Silicon Graphics computer

(O2) and presented on a LG Studioworks 221U Monitor

(1152� 870 pixel, monitor size 40� 30.2 cm), viewed froman observation distance of 50 cm with frame frequency of

75 Hz. The screen contained overall 50% white and 50%

black pixels. The target for both conditions was 28 high and 48wide, and moved for 2 s at a speed of 68/s from bottom

upwards or from the top down. AM and 21 age-matched

control subjects (mean age of 43 years, minimum age of 38,

maximum age of 54 years) were tested. Subjects were seated

in a dimly lt room and were instructed to fixate a centralsmall red arrow (1.38) that indicated whether the target would

appear on the left or right side of the screen. Subjects had

to indicate verbally whether the rectangle seemed to move

upwards or downwards (a binary forced choice task). The

examiner entered the responses on the keyboard without

seeing the stimulus. False answers were followed by acoustic

feedback. For both hemifields 50 trials were presented each

and coherence level was controlled using a staircase pro-cedure (PEST; Taylor and Creelman, 1967). To determine

thresholds for motion perception, PEST varied the percentage

of dots within the stimulus area, by gradually decreasing the

percentages of dots within the rectangle that moved in the

defined direction, starting with a correlation of 100%. Hence,

with 0% correlation the movements of the dots within the

rectangle were absolutely identical to those in the surrounding

and the target was no longer present. Direction discriminationthresholds, defined as percentage of signal dots that lead to

75% correct responses, were calculated using probit analysis

(Finney, 1962).

Motion detection did not differ significantly between hemi-

fields both in AM and in the control group, hence we averaged

the thresholds for the left and right sides (see Table 3).

AM was severely impaired in second order motion perception,as he scored 4 standard deviations above the threshold of

the healthy controls. His first order motion perception was

somewhat better and at least one of the control subjects

performed of the same level (see Table 3).

Visual evoked potentials

Cortical potentials (VEP) were evoked by presenting a

contrast-reversing checkerboard pattern, either achromatic

white/black or else chromatic blue/red. In the control conditionthe size of each square element was 1.5 cm. In the experimental

condition element size was 10 cm. AM was positioned in a

darkened room at a distance of 1 m from the screen of a 14-

inch VGA monitor. The elements of the checkerboard there-

fore comprised 0.868 in the control condition and 5.78 in the

experimental condition. An additional stimulus consisted of a

black/white checkerboard with very small elements. The first

set of VEPs (t1) started with these small elements (0.438),continued with the control condition (0.868), and ended with

the experimental condition (5.78). In the achromatic series

Table 3. Thresholds of AM and controls in detecting first-order (Fourier) andsecond-order (Theta) motion

Fourier motiona Theta motiona

Controls (n¼ 21)Mean 32.85 36.39Standard Deviation 5.82 6.77Minimum 25.20 26.6Maximum 45.85 47.10

AM: t1 45.85 74.05AM: t2 – 63.6

aNumbers indicate the percentages of dots moving coherently in the target area,necessary for discrimination of motion direction. Thresholds of the left and righthemifield are averaged.

Fig. 3. VEP for different, chromatic and achromatic spatial layouts in AM.Left side: VEP for left eye stimulation. Right side: VEP for right eyestimulation. Each stimulation was replicated two times producing two graphsper panel. Note the reduced or almost absent VEPs for both eyes in theachromatic condition with low spatial frequency patterns (lower panels).

Differential impact of parvocellular and magnocellular pathways 211

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AM evoked a normal VEP in the small-sized and in the control

conditions, but there was no clear P100 in the experimental

condition. Because of a possible order effect, we replicated

the experimental condition in reverse order after two days (see

Fig. 3 and t2 in Table 4) and again seven weeks later (t3 in

Table 4). At t1 there was no clear-cut N1/P100 complex. At t2 apeak-to-peak amplitude (N1/P100) of 2.6mV was measured

for the left eye and 2.45mV for the right eye. At t3 the

corresponding amplitudes were 4.3mV and 2.2mV. With the

exception of the amplitude for the left eye at the last measure-

ment, all amplitudes were completely outside the range of an

age-matched control group (n¼ 17, mean age of 47, minimum

age of 38, maximum age of 60 years). During stimulation by

chromatic reversals the size of the checkerboard elements didnot influence the results. In both conditions, AM showed a

pronounced P100, within the range of the control group (see

Table 4). Therefore, AM’s reduction of the peak-to-peak am-

plitude was specific for the large sized black/white checker-

board.

The latencies of the P100 of AM were prolonged in each of

the black/white reversal conditions, but not in the color

reversals.

Discussion

Visual form agnosia has been documented in the past in

several case descriptions of patients suffering from hypoxia,

carbon monoxide poisoning, or bilateral posterior infarcts.Our patient AM suffered from a sudden heart arrest. His

visual and memory impairment were therefore caused by

brain hypoxia although no morphological brain damage

could be traced on an MRI two months after the event.

The profile of his impairments was similar to that of the

case SMK of Davidoff and Warrington (1993), while he

was somewhat less impaired than the case of Milner et al.

(1991). The similarity of our case with SMK is striking.Like SMK, AM was able to perceive subjective contours,

colors and individual geometrical objects, but he could not

give exact size estimations. In both cases the reading ability

was highly impaired and both had problems recognizing

objects in their environment, especially drawings and pic-

tures without color information. On the other hand, while

SMK was able to trace overlapping figures, AM was un-

able to do so. In this respect, AM resembles FGP more

(Kartsounis and Warrington, 1991), who also had problemsrecognizing both overlapping and embedded figures. But

FGP was able to discriminate between different object

sizes, while AM had problems with this task. The visual

impairment of AM is an additional argument for the

existence of independent mechanisms for figure/ground

discrimination on one hand and the perception of the re-

lative size of surfaces on the other. FGP was able to give a

correct size estimation, while SMK and AM could not.From a functional neuroanatomical viewpoint it can be

argued that V1 and V2 have to be intact in AM. In case of

a lesion of V1 one would expect visual field deficits and an

attenuation of the VEP potentials. This was not the case in

AM. V2 is concerned with higher order boundary percep-

tion. Peterhans and von der Heydt (1989, 1991) have shown

that neurons in this part of the visual system of monkeys

are activated by illusionary contours presented in theirreceptive fields. Because AM was able to detect such

patterns and to discriminate between different Kanisza

figures, V2 presumably was not impaired by the hypoxia.

This assumption can also be illustrated by the fact of

AM’s abilities to identify letters and short words if printed

in an appropriate font type. Zeki et al. (1990) and Barbur

et al. (1993) have shown that V4 is a major centre of

conscious color perception. Again, at least some parts ofV4 must have been spared from the hypoxia, because AM

was able to discriminate between colors easily and showed

a normal checkerboard VEP based on blue/red reversals.

The main functional problem for AM was to separate figure

from ground, to separate individual letters in reading, and to

estimate sizes. We would like to argue that his impaired

performance in the visual and spatial location tasks of the

VOSP can also be explained by the latter impairment, becauseboth tasks rely on locating stimuli relative to a background

Table 4. Results of the VEP investigation

Black/white Blue/red

High spatial frequency Low spatial frequency High spatial frequency Low spatial frequency

Left eye Right eye Left eye Right eye Left eye Right eye Left eye Right eye

Control (n¼ 17)sMean 9.35 8.76 6.61 6.12 6.78 6.48 6.25 6.78SD 3.68 4.24 2.59 3.06 2.32 2.29 2.28 2.90Maximum 18.32 20.50 13.23 13.20 10.70 11.50 9.68 9.68Minimum 3.52 3.08 3.71 2.90 2.10 3.86 1.96 3.17

AM: t1 3.26 1.54 0.91 1.89AM: t2 6.81 7.08 2.60 2.45 6.02 4.87 6.27 4.60AM: t3 5.16 6.23 4.30 2.20

All figures: peak to peak mV differences of N1/P100.

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figure (the squares). Kartsounis and Warrington (1991) and

Milner et al. (1991) assumed that the impairment of FGP and

DF might be due to a lesion of the magnocellular pathway.

Such a hypothesis would be too general for AM because he

(like DF) was able to walk, to grasp and to localize objects in

the environment. All these performances rely on precise

visual-spatial perception. Furthermore, AM was able to copy

reasonably well (although not in the normal range), whichalso argues for an intact perception of spatial coordinates.

Motion perception is certainly one of the major functions of

the magnocellular system and recently Braddick et al. (2003)

proposed tests of global motion processing, i.e., the detection

of coherently moving dots, as an appropriate means to analyse

‘‘dorsal stream vulnerability.’’ In their view the relative

threshold increase (how many dots have to move coherently

in a specific area for a predominant direction being seen)may be a sensitive measurement of the integrity of the

magnocellular system.

We used two such tests – one for first-order and one for

second-order motion perception – to investigate AM’s motion

perception abilities. In both tests AM scored more than two

standard deviations above – i.e., worse than – the control

group, and at least in the second-order motion task his

performance was completely outside the range of the controlgroup. This result points to an impairment of the magnocel-

lular system, especially in the processing of higher-order

motion signals, which presuppose a decoupling of local

directional selectivity at V1 from the direction of a globally

moving object.

On the other hand, one could argue that the deficit in motion

perception of AM is not necessarily the result of a defect of

magnocellular neurons but may also be a consequence of hisvisual form agnosia. We did not notice any clinical impairment

in motion perception and, although AM could identify surfaces

of degraded stimuli such as the ‘‘X’’ in the screening test of the

VOSP, he was not perfect in this task. Detecting the predo-

minant motion direction of more or less coherently moving

dots involves a similar perceptual function as in the screening

test of the VOSP. Therefore, a subclinical impairment

obviously led to a significant deficit in the motion perceptiontask, with its more extended area to integrate and lower

coherence level which make detection much more difficult.

It has been argued that another function of the magnocel-

lular system is the selection of items within arrays of similar

items (Omtzigt et al., 2002). While the parvocellular system

identifies the feature in the focus of attention, the magnocel-

lular system identifies, according to this hypothesis, the global

structure in which this feature is embedded. Such a view of themagnocellular system has been used to explain dyslexia as an

impairment of the magnocellular system (Livingstone et al.,

1991; Sperling et al., 2003; Stein, 2003). AM was not only

dyslexic, he also resembled dyslexic children in two other

respects, which are considered as a sign for a magnocellular

deficit (Stein, 2003). First, he had problems in higher-order

motion perception (see above) and second, he showed a ‘‘left

minineglect’’ (Hari et al., 2001) as he was about 120 ms

slower in responding to targets in the left hemifield compared

to the right hemifield.

If integration of different focal aspects into one global pic-

ture relies on magnocellular structures, the investigation of

the visual evoked potential is also of relevance. AM’s

amplitudes in the black/white reversal VEPs for coarse

checker-boards were subnormal while normal for colored

checker- boards of all element-sizes. Hence, the deficit seemsto be specific for large receptive fields, low spatial frequency

stimulus, i.e., a coarse checkerboard, evokes a normal VEP

amplitude for a chromatic pattern while an impaired VEP for

an achromatic pattern. This dissociation could be explained

by the involvement, in the first case, of parvocellular struc-

tures, whereas this is not the case primarily in the achromatic

condition. The investigations of Tobimatsu et al. (1995) and

Arakawa et al. (1999) demonstrate that achromatic stimula-tion of the parvocellular pathway can be dissociated from

chromatic stimulation using different spatial frequencies.

Higher achromatic spatial frequencies (more than 2 cycles

per degree) seem to stimulate primarily the parvocellular

interblob pathway, whereas low frequency spatial patterns

have a higher impact on magnocellular structures, as demon-

strated in research on reading and neglect (Spinelli et al.,

1996).The comparatively better ability of AM to recognize draw-

ings of animals, compared to drawings of manmade objects,

may also be explained by such a difference between the

parvocellular and the magnocellular system, while, of course,

other explanations are possible. Animal pictures, as in the

Snodgrass and Vanderwart (1980) drawings, often possess

typical features, which allow identification irrespectively of

their global shape. Manmade objects like tables, chairs, etc. arecharacterized as drawings by symmetrical and partly over-

lapping features. Recognition therefore presupposes a global

integration of local features. In summary we suggest that the

visual deficits of AM may be caused primarily by a defect of

the magnocellular system as a result of the anoxic episode.

Acknowledgement

We would like to thank Paul Eling (Nijmegen) and Manfred

Fahle (Bremen) for their comments on an earlier draft of this

article.

Supported by German Research Council, SFB 517.

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